And Apion Sp

Available online at www.sciencedirect.com

Biological Control 43 (2007) 317–322 www.elsevier.com/locate/ybcon

Ecology and impact of Allorhogas sp. (Hymenoptera: Braconidae) and Apion sp. (Coleoptera: Curculionoidea) on fruits of Miconia calvescens DC (Melastomataceae) in Brazil

Francisco R. Badenes-Perez a,*, M. Tracy Johnson b

a Paciﬁc Cooperative Studies Unit, University of Hawaii at Manoa, Honolulu, HI 96822, USA b Institute of Paciﬁc Islands Forestry, USDA Forest Service, PSW Research Station, Volcano, HI 96785, USA

Received 19 April 2007; accepted 23 August 2007 Available online 1 September 2007

Abstract

Two fruit-feeding insects, a gall wasp, Allorhogas sp. (Hymenoptera: Braconidae), and a beetle, Apion sp. (Coleoptera: Curculionoi- dea), were evaluated in their native habitat in Brazil as potential biological control agents of Miconia calvescens DC (Melastomataceae). Allorhogas sp. occurred at two out of three field sites with native populations of M. calvescens, and Apion sp. occurred at all three sites. Both species exhibited aggregated distributions among M. calvescens trees sampled at each site. Allorhogas sp. infested 9.0% and 3.8% of fruits at each of two sites. The number of larvae and pupae of Allorhogas sp. and/or an unidentified parasitoid (Hymenopetera: Eulo- phidae: Tetrastichinae) ranged from one to five per infested fruit. Fruits infested with Allorhogas sp. were 20% larger and had 79% fewer seeds than healthy fruits. Although adults of Apion sp. were found on leaves and inflorescences of M. calvescens at all three sites, larvae and pupae were found in fruits at only one site, where a maximum of 1.4% of fruits were infested. Fruits infested by Apion sp. contained only one larva or pupa, and were 15% smaller and had 62% fewer seeds than healthy fruits. While a variety of apionids have been used for biological control in the past, this is the first time a braconid wasp has been considered for biological control of a weed. 2007 Elsevier Inc. All rights reserved.

Keywords: Miconia calvescens; Phytophagous gall wasp; Allorhogas; Apion; Weed management; Seed; Fruit size

1. Introduction Medeiros et al., 1997). Biological control is considered an essential tool for long term management of M. calvescens The velvet tree, Miconia calvescens DC (Melastomata- (Smith, 2002). Classical biological control of weeds via ceae), is a small tree native to Central and South America the introduction of natural enemies from the native habitat that is considered a serious threat to natural ecosystems in of the weed is one of the most important methods to man- Hawaii and other Pacific islands because of its ability to age alien invasive weeds (Denslow and Johnson, 2006; invade intact forests of these islands, having already dis- Julien and Griffiths, 1998). Prerelease studies in the native placed over 65% of the native forest in Tahiti (Medeiros habitat of the invasive weed can be challenging to conduct, et al., 1997; Meyer, 1998; Meyer and Florence, 1996). Her- yet are fundamental to assess the potential of biological bicidal and mechanical removal are the main methods used control agents (Goolsby et al., 2006). to contain the spread of M. calvescens, but control is diffi- The success of M. calvescens as an invasive plant is partly cult and costly, especially in remote areas (Kaiser, 2006; due to its prolific reproduction, with one mature tree flowering up to 3 times per year and bearing up to 220 inflorescences that can produce more than 200 fruits each with 25–200 * Corresponding author. Present address: Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, D-07745 seeds per fruit (Medeiros et al., 1997; Meyer, 1998). The Jena, Germany. Fax: +49 0 3641 57 1502. impact of seed feeders in weed biocontrol has yielded mixed E-mail address: [email protected] (F.R. Badenes-Perez). results (Goolsby et al., 2006). Seed-feeders are sometimes

1049-9644/$ - see front matter 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2007.08.007 318 F.R. Badenes-Perez, M. Tracy Johnson / Biological Control 43 (2007) 317–322 considered useful biological control agents of weeds only in Guaraciaba, and Viçosa, all in the state of Minas Gerais. seed-limited plant systems (Crawley, 1992; Myers, 1978). In Minas Gerais is the southeastern part of Brazil (Planalto the case of M. calvescens, even if it is not seed-limited, since it Central) and the region is noted for tropical climate and is dispersed by birds feeding on fruit and a sufficient measure hilly terrain. Field sites were in secondary Atlantic forest of biological control success could be to reduce its spread, heavily disturbed by adjacent agricultural and eucalyptus insects that feed on inflorescences and/or fruits of M. calves- plantations. The area sampled in each field site was approx- cens could help managing this weed. Apion spp. (Coleoptera: imately 1 ha and contained 15–35 adult plants bearing infl- Curculionoidea) and relatives, have been used with some orescences depending on the site. Distance between M. success in some cases of biological control of weeds in Cyti- calvescens plants was highly variable, some plants being sus scoparius (L.), Emex spp., Mimosa pigra L. and Ulex right next to each other and others several hundred meters europaeus L. (Julien and Griffiths, 1998; McClay and De apart. Altitude for Dionı´sio, Guaraciaba, and Viçosa is Clerck-Floate, 1999), but not in others (e.g., Hill et al., 345, 570, and 645 m above sea level, respectively. Distances 1991). The species of Apion studied here was suggested as a between the field sites were approximately 120 km between possible seed-feeder associated with M. calvescens after Dionı´sio and Guaraciaba, 145 km between Dionı´sio and being found on M. calvescens leaves (Picanço et al., 2005). Viçosa, and 60 km between Guaraciaba and Viçosa. While dissecting fruits to confirm the presence of Apion sp. larvae in M. calvescens fruits and to assess their impact on 2.2. Insect abundance M. calvescens fruit, we accidentally found Allorhogas sp. and we also included it in the study. The genus Allorhogas 2.2.1. Apion sp. adults on inflorescences and leaves is distributed worldwide and was once presumed, like all Bra- To assess abundance and distribution of Apion sp., infl- conidae, to be exclusively parasitic of other insects (Maceˆdo orescences and leaves of M. calvescens were sampled at and Monteiro, 1989; Shenefelt and Marsh, 1976). Since the each of the three field sites. In April 2006, five inflorescences first phytophagous braconid was documented by Maceˆdo in each of 10 randomly selected trees at each site were sha- and Monteiro (1989), other cases of plant feeding Hymenop- ken individually over a 40 · 20 · 10 cm white plastic tray to tera have been described and gall-inducing species have been dislodge and collect Apion sp. adults. In June 2006, leaves reported in Brazil and Costa Rica on the plant genus Conos- were examined in 10 randomly selected trees at each site, tegia (Melastomataceae), Pithecellobium (Fabaceae), and and all adult beetles were collected with an aspirator. Stryphnodendron (Fabaceae) (Austin and Dangerfield, Vouchers specimens were deposited in the Zoology 1998; Infante et al., 1995; Maceˆdo and Monteiro, 1989; Museum of the Department of Biology at the University Marsh et al., 2000; Wharton and Hanson, 2005). Addition- of Costa Rica. ally, here we report a gall inducing Allorhogas sp. on the genus Miconia (Melastomataceae). Although no detailed 2.2.2. Allorhogas sp. and Apion sp. larvae/pupae in fruit studies have been completed on most gall-forming Allorho- To assess abundance and distribution of Allorhogas sp. gas spp., early taxonomic evaluation suggests that they rep- and Apion sp. in fruits of M. calvescens, five fruiting inflo- resent a highly diverse group with each species being quite rescences were collected at random from each of 10 ran- host specific (Hanson, personal comment). Gall formers domly selected trees at each site. Inflorescences were are considered relatively successful biological control agents brought to the laboratory where 10 fruits were randomly of weeds because of their impact on plant development (galls selected from each inflorescence for dissection and exami- act as resource sinks) and reproduction as well as their host nation with a stereomicroscope. The number of larvae specificity (Dennill et al., 1999; Harris and Shorthouse, and pupae of Allorhogas sp. and Apion sp. in each fruit 1996; Hoffmann et al., 2002; Julien and Griffiths, 1998; was recorded. Presence of an undescribed eulophid parasit- Meyer, 1987; Morris, 1999; Weiss et al., 1988). oid (Hymenopetera: Eulophidae: Tetrastichinae) attacking The main objectives of this research were to study abun- Allorhogas sp. also was recorded. Fruits were sampled on dance and within-tree dispersion of Allorhogas sp. and 21–23 August 2006 at the three field sites. On 14 September Apion sp. on M. calvescens in their native habitat in Brazil 2006, fruit sampling was repeated at the Viçosa site, where and to determine their effect on M. calvescens fruit size and fruit development lagged behind the other sites, probably seed set. We hypothesize that these species may have a due to lower temperatures in Viçosa. At the time of sam- significant impact in reducing seed set in M. calvescens,in pling, each inflorescence was assigned to one of four phe- which case they would deserve further attention as poten- nological categories: <25%, 25–50%, 50–75%, and >75% tial biological control agents. mature (red or purple) fruit.

2. Materials and methods 2.3. Impact of Allorhogas and Apion sp. on fruit

2.1. Study sites To quantify the effect of Allorhogas sp., fruit diameter and the number of seeds per fruit were determined in a This study was conducted in three different locations in total of 40 fruits (including fruits infested and non-infested the native habitat of M. calvescens in Brazil: Dionı´sio, with Allorhogas sp.) randomly selected from five infested F.R. Badenes-Perez, M. Tracy Johnson / Biological Control 43 (2007) 317–322 319 fruiting inflorescences collected on three different plants at tively. Apion sp. adults exhibited aggregated distributions the Dionı´sio field site on 21 August 2006. The effect of Api- among M. calvescens trees at all sites (Table 1). on sp. on M. calvescens fruits was quantified as fruit diameter and the number of seeds per fruit in a total of 20 fruits 3.1.2. Allorhogas sp. and Apion sp. larvae/pupae in fruit (10 healthy fruits and 10 fruits infested with Apion sp. lar- Allorhogas sp. and/or its parasitoid infested 9.0% and vae and/or pupae) randomly selected from five infested 3.8% of dissected fruits from Dionı´sio and Guaraciaba, fruiting inflorescences collected on three different plants respectively, while no Allorhogas sp. was found in Viçosa. at the Viçosa field site on 23 August 2006. The number of larvae and pupae of Allorhogas sp. and/ or its parasitoid ranged from 1 to 5 per infested fruit, with 2.4. Statistical analysis an average of 2.7 and 2.8 insects per infested fruit at Dionı´- sio and Guaraciaba, respectively. No Apion sp. larvae/ Dispersion of insects was assessed after determining pupae were found in fruits from Dionı´sio and Guaraciaba insect abundance by calculating the means and variance despite observations of scars produced by Apion sp. adults of each population sampled as number of insects per tree feeding on M. calvescens fruits and presence of Apion sp. for each field site. A variance to mean ratio equal to one adults on leaves and inflorescences at those field sites. At indicates a random dispersion, <1 indicates a uniform dis- Viçosa, only one Apion sp. larva was found in one fruit persion, and >1 indicates an aggregated dispersion (Davis, during the first sampling on 23 August 2006, while 1.4% 1994; Myers, 1978). To determine the relationships of fruits were infested by Apion sp. larvae on the second between number of Allorhogas sp., parasitized and not, sampling on 14 September 2006. Infested fruits never con- and fruit size and number of seeds per fruit, stepwise multi- tained more than a single larva or pupa of Apion sp. ple regression analyses were performed with the PROC Samples of immature Allorhogas sp. and Apion sp. in REG procedure of SAS (SAS Institute Inc., 2004). When fruit showed aggregation among trees, evidenced by vari- significant treatment differences were indicated by a signif- ances far exceeding mean densities for Allorhogas sp. in icant F-test at P 6 0.05, means were separated by Fisher’s particular (Table 2). Fruits infested with Allorhogas sp. Protected least significant difference (SAS Institute Inc., were found in only five and three out of the 10 trees sam- 2004). Data comparing fruit size and number of seeds in pled at Dionı´sio and Guaraciaba, respectively. Among healthy fruits and fruits affected by Apion sp. were analyzed infested trees, 40% and 60% of inflorescences contained using a paired t-test with the PROC TTEST procedure of infested fruits, and within infested inflorescences, 48% SAS (SAS Institute Inc., 2004). In order to normalize and 32% of fruits contained Allorhogas sp. at Dionı´sio the residuals, a square root (x) function was used for trans- and Guaraciaba, respectively. Fruits infested with Apion formation of all data. Although tests of significance for sp. were found in only three of the 10 trees sampled at Viç- these analyses were based on the transformed data, only osa, with 33% of inflorescences in infested trees containing untransformed data are presented. infested fruits and 33% of fruits in infested inflorescences containing Apion sp. 3. Results Inflorescences sampled from Dionı´sio and Guaraciaba contained >75% mature fruits. At Viçosa, inflorescences 3.1. Insect abundance and distribution consisted of <25% and 25–50% mature fruits during the first and second sample periods, respectively. 3.1.1. Apion sp. adults on inflorescences and leaves An average of 0.7, 2.7 and 0.5 adults per tree were 3.2. Impact of Allorhogas and Apion sp. on fruit observed in inflorescences sampled in April 2006 at Dionı´- sio, Guaraciaba, and Viçosa, respectively. An average of Fruit diameter increased linearly with number of Allo- 0.8, 1.4 and 0.3 adults per tree were observed on M. calves- rhogas sp. and its parasitoid per fruit (n =40, r2 = 0.50, cens leaves (usually on the abaxial side of leaves) sampled F = 37.21, P < 0.001) (Fig. 1). Fruits infested with Allorho- in June 2006 at Dionı´sio, Guaraciaba, and Viçosa, respec- gas sp. were an average of 20% larger than healthy fruits

Table 1 Mean number and variance of Apion sp. adults in leaves and inflorescences of M. calvescens in three locations (Dionı´sio, Guaraciaba and Viçosa) in its native habitat in Brazil Site Insects per tree on leaves Insects per tree on inflorescences Sampling date Mean ± SEM Variance/Mean Sampling date Mean ± SEM Variance/Mean Dionı´sio June 21, 2006 0.8 ± 0.4 2.1 April 27, 2006 0.7 ± 0.5 3.8 Guaraciaba June 21, 2006 1.4 ± 0.7 4.0 April 27, 2006 2.7 ± 1.4 7.3 Viçosa June 19, 2006 0.3 ± 0.2 1.5 April 25, 2006 0.5 ± 0.3 2.3 A variance to mean ratio >1 was used as an indication of an aggregated distribution (Davis, 1994; Myers, 1978). A total of 10 trees sampled to determine insects on leaves and a total of 50 inflorescences (5 inflorescences for each of 10 trees) sampled to determine insects on inflorescences. 320 F.R. Badenes-Perez, M. Tracy Johnson / Biological Control 43 (2007) 317–322

Table 2 Mean number and variance of Apion sp. and Allorhogas sp. larvae and pupae in fruits of M. calvescens in three locations (Dionı´sio, Guaraciaba and Viçosa) in their native habitat in Brazil Site Sampling date Apion sp. Allorhogas sp/ % of fruit infested Insects per tree % of fruit infested Insects per tree Mean ± SEM Variance/Mean Mean ± SEM Variance/Mean Dionı´sio August 21, 2006 0.0 0.0 — 9.0 12.9 ± 5.5 23.6 Guaraciaba August 22, 2006 0.0 0.0 — 3.8 5.5 ± 3.8 26.7 Viçosa August 23, 2006 0.1 0.1 ± 0.1 1.0a 0.0 0.0 — Viçosa September 14, 2006 1.4 1.0 ± 0.5 2.9 0.0 0.0 — A variance to mean ratio > 1 was used as an indication of an aggregated distribution (Davis, 1994; Myers, 1978). A total of 50 inflorescences (5 inflorescences for each of 10 trees) sampled to determine insects on inflorescences. a Since only one Apion sp. larva was found during the sampling in August 2006, this datum was not taken into account to analyze the distribution of Apion sp.

7 the number of seeds by 79% compared to healthy fruits (average number of seeds in infested fruits was 14.7 ± 3.5 6 versus 69.9 ± 8.6 in healthy fruits). 5 There were signiﬁcant diﬀerences in fruit size (t = 3.44, df = 18, P = 0.003) and number of seeds per fruit 4 (t = 5.87, df = 18, P < 0.001) between healthy fruits and 3 fruits infested by Apion sp. Fruits infested with Apion sp.

Fruit size (mm) were 15% smaller than healthy fruits (average diameter of 2 infested fruits was 3.60 ± 0.12 mm versus 4.22 ± 0.13 mm

1 in healthy fruits), while number of seeds per fruit was 62% lower in infested than in healthy fruits (average num- 0 0 2345ber of seeds in infested fruits was 45.5 ± 9.5 versus 1 Total number of insects (Allorhogassp. + eulophid parasitoid) 119.3 ± 8.2 in healthy fruits). per M. calvescens fruit

Fig. 1. Relationship between number of Allorhogas sp. and eulophid 4. Discussion parasitioids per fruit and fruit size in M. calvescens fruits collected in Dionı´sio, Brazil (ﬁtted line: y = 3.97 + 0.31 x). We present here an initial assessment of two potential agents for biological control of M. calvescens. Ours is the 140 ﬁrst study of fruit-feeding herbivores of M. calvescens in

120 Brazil, and the first discovery of Allorhogas sp. attacking this important weed. Gall-forming Allorhogas spp. have 100 been found recently in fruits of several other Miconia 80 spp. in Costa Rica, but never in M. calvescens despite 60 intensive sampling of fruits (Chacoń, unpublished). Devel- 40 opment of Allorhogas sp. as a biological control agent for M. calvescens would constitute the first use of a braconid Number of seeds per fruit 20 wasp in classical biological control of weeds. 0 012345Adults of Apion sp. have been collected previously on Total number of insects (Allorhogas sp. + eulophid parasitoid) M. calvescens leaves in Brazil and were presumed to be per M. calvescens fruit feeding in M. calvescens inflorescences (Picanço et al., Fig. 2. Relationship between number of Allorhogas sp. and eulophid 2005). Here we confirm larval development of Apion sp. parasitioids and number of seeds per fruit in M. calvescens fruits collected in M. calvescens fruits. The presence of Apion sp. on M. in Dionı´sio, Brazil (fitted line: y = 16.3 À 5.8 lnx). calvescens inflorescences is likely due to oviposition and feeding, as it happens with A. ulicis in U. europaeus inflo- (average diameter of infested fruits was 4.74 ± 0.15 mm rescences (Hoddle, 1991; Norambuena and Piper, 2000). versus 3.96 ± 0.08 mm in healthy fruits. A logarithmic It is not known whether the Apion sp. adults found on function was the best to describe the relationship between M. calvescens leaves were just resting and taking shelter number of Allorhogas sp. and its parasitoid and the number or whether they also feed on leaves, but no obvious signs of seeds per M. calvescens fruit (n = 39 – one obvious out- of feeding on leaves was observed during the sampling lier discarded, r2 = 0.60, F = 20.76, P < 0.001) (Fig. 2). (Badenes-Perez, personal observation). Although inflores- Presence of Allorhogas sp. in M. calvescens fruits reduced cences of M. calvescens develop asynchronously (e.g., F.R. Badenes-Perez, M. Tracy Johnson / Biological Control 43 (2007) 317–322 321 different development stages found within a plant and even Allorhogas sp. may also have increased permanence in the within an inflorescence) and plants flower twice a year in tree, as the higher rates of Allorhogas sp. infestation were the field sites studied, there seems to be a period of several found in trees with an advanced plant phenology (with months where there may be very few, if any, inflorescences most fruits mature) and with relatively few fruits left on available. Thus, since Apion sp. adults have been collected the tree (Badenes-Perez, personal observation). year-round on M. calvescens (Picanço et al., 2005), they Significant seed reduction caused by both Apion sp. and may be able to utilize resources other than inflorescences Allorrhogas sp. and possible early abscission of fruits and/or may be feeding in other hosts other than M. calves- affected by Apion sp. show that both species deserve further cens during that time. study to assess their potential as biological control agents Allorhogas sp. and Apion sp. showed an aggregate dis- of M. calvescens. Further research is also necessary to persion across M. calvescens plants. Aggregated distribu- study the biology of Apion sp. and Allorhogas sp. Although tions of organisms are widespread in nature, and another other Apion spp. have been shown to be univoltine in Apion sp., A. onopordi Kirby, has also been shown to fol- plants flowering once a year (Freese, 1991; Hoddle, 1991; low an aggregated distribution on host plants (Moravie Scott and Yeoh, 2005), the number of generations per year et al., 2006). Phenology across trees was quite similar at in this Apion sp. could be two because there are two distinct the time of the sampling (Badenes-Perez, personal observa- flowering periods in M. calvescens at the field sites studied. tion), indicating that phenology is not an important vari- Additional research would also be necessary to test the able for aggregation at a given time. Differences in influence of factors associated with location (e.g., plant abundance of Allorhogas sp. and Apion sp. were found in phenology) on population densities of Allorhogas sp. and the different field sites sampled in Dionı´sio, Guaraciaba, Apion sp. and to test the effect of these insects on fruit per- and Viçosa, but since we only sampled once in Dionı´sio manence in M. calvescens plants. We do not know what and Guaraciaba (corresponding to one frutescence phenol- level of reduction in fruits/seeds of M. calvescens is neces- ogy), and twice in Viçosa (corresponding to two different sary to significantly decrease the spread of populations, frutescence phenologies), we cannot make inferences on as other factors, such as availability of space adequate what factors were responsible for the observed differences for plant growth and dispersal agents (e.g., birds) may be in insect densities. Among the many factors associated with important limiting factors in M. calvescens dispersal. A a geographical location, we hypothesize that the effect of related species, A. ulicis has not significantly reduced gorse climatic differences between sampling sites (e.g., higher ele- invasiveness in Chile and New Zealand despite reducing vation and colder temperatures in Viçosa than in Dionı´sio seed production significantly (Hill et al., 1991; Norambue- and Guaraciaba), had an effect on the densities of Allorho- na et al., 1986, 2007). Given the reproductive and invasive gas sp. and Apion sp. due to their effect on inflorescence capacity of M. calvescens, besides fruit feeders, other bio- phenology (more advanced in Dionı´sio and Guaraciaba logical control agents affecting other parts of the plant, than in Viçosa at the times when sampling was conducted). such as insect defoliators, could be used simultaneously Fruits infested with Allorhogas sp. were found when >75% to improve management of M. calvescens (Badenes-Perez of fruits were mature and fruits infested with Apion sp. and Johnson, 2007). The effectiveness of Allorhogas sp. were found when 25–50% of fruits were mature (except and Apion sp. as biological control agents of M. calvescens for one insect found when <25% fruits were mature), indi- in a particular habitat would depend on how favorable or cating that plant phenology could be an important factor antagonistic the environment is to the growth and repro- determining the abundance of these insects in M. calvescens duction of the insects. Climatic differences between the fruits. The effect of plant phenology in oviposition prefer- native habitat of the insects and Hawaii should be assessed. ence is well-known in many insect groups (e.g., Badenes- Parasitoids and predators are the main source of mortality Perez et al., 2005), including Apion spp., as A. ulicis, has among insect gall makers, tending to be as specialized as been shown to preferentially attack 10- to 35-day-old pods the gall makers themselves (Weiss et al., 1988). Since there of gorse (Hoddle, 1991). Infestation by Allorhogas sp. and are no Allorhogas spp. in Hawaii, natural enemies of Allo- Apion sp. could also affect fruit permanence in the tree. rhogas sp. are likely to be absent there. Experiments to test Infestation of M. calvescens by Apion sp. may have resulted host specificity on Allorhogas and Apion sp. would be nec- in premature abscission of the fruit, as fruits affected by essary to further study the potential of these insects as bio- Apion sp. tended to be smaller than healthy fruits, indicat- logical control agents of M. calvescens. ing an irregular development in fruits infested by Apion sp. Another curculionid feeding on M. calvescens seeds, Ant- Acknowledgments honomus monostigma Champion (Coleoptera: Curculioni- dae), seems to produce early abscission of M. calvescens We thank Drs. Robert Barreto, and Marcelo Picanço as fruits (Chacoń, unpublished). Early abscission of fruits well as people working in their laboratory groups at the affected by Apion sp. would make Apion sp. larvae less Universidade Federal de Viçosa, especially Dr. Marcio likely to appear when sampling, which could explain why Dionizio and Elisangela Fidelis de Morais, for assistance fruits infested with Apion sp. larvae were not very common conducting this study. We also thank Dr. Paul Hanson at despite higher presence of Apion sp. adults. Galling by the Universidad de Costa Rica for help with insect 322 F.R. Badenes-Perez, M. Tracy Johnson / Biological Control 43 (2007) 317–322 identification and for providing helpful comments on the Marsh, P.M., Maceˆdo, M.V.d., Pimental, M.C.P., 2000. Description and initial draft of the manuscript. Funding was provided by biological notes on two new phytophagous species of the genus the Hawaii Invasive Species Council and the US Forest Allorhogas from Brazil (Hymenoptera: Braconidae: Doryctinae). Journal of Hymenoptera Research 9, 292–297. Service International Programs. McClay, A., De Clerck-Floate, R., 1999. Establishment and early effects of Omphalapion hookeri (Kirby) (Coleoptera: Curculionidae) as a bio- References logical control agent for scentless chamomile, Matricaria perforata Merat (Asteraceae). Biological Control 14, 85–95. Austin, A.D., Dangerfield, P.C., 1998. Biology of Mesostoa kerri Austin Medeiros, A.C., Loope, L.L., Conant, P., McElvaney, S., 1997. Status, and Wharton (Insecta: Hymenopterae: Braconidae: Mesostoinae), an ecology and management of the invasive plant Miconia calvescens DC endemic Australian wasp that causes stem galls on Banksia marginata (Melastomataceae) in the Hawaiian Islands. Bishop Museum Occa- Cav. Australian Journal of Botany 46, 559–569. sional Papers 48, 23–36. Badenes-Perez, F.R., Johnson, M.T., 2007. Ecology, host specificity and Meyer, J.-Y., 1998. Observations on the reproductive biology of Miconia impact of Atomacera petroa Smith (Hymenoptera: Argidae) on calvescens DC (Melastomataceae), an alien invasive tree on the island Miconia calvescens DC (Melastomataceae). Biological Control 43, of Tahiti (South Pacific Ocean). Biotropica 30, 609–624. 95–101. Meyer, J.-Y., Florence, J., 1996. Tahiti’s native flora endangered by the Badenes-Perez, F.R., Nault, B.A., Shelton, A.M., 2005. Manipulating the invasion of Miconia calvescens DC (Melastomataceae). Journal of attractiveness and suitability of hosts for diamondback moth (Lepi- Biogeography 23, 775–781. doptera: Plutellidae). Journal of Economic Entomology 98, 836–844. Meyer, J., 1987. Plant galls and gall inducers. Borntraeger, Berlin, Crawley, M.J., 1992. Seed predators and plant population dynamics. In: Germany. Fenner, M. (Ed.), Seeds: The Ecology of Regeneration in Plant Moravie, M.-A., Borer, M., Bacher, S., 2006. Neighbourhood of host Communities. CAB International, Wallingford, UK, pp. 157–192. plants influences oviposition decisions of a stem-boring weevil. Basic Davis, P.M., 1994. Statistics for describing populations. In: Pedigo, L.P., and Applied Ecology 7, 545–554. Buntin, G.D. (Eds.), Handbook of Sampling Methods for Arthropods Morris, M.J., 1999. The contribution of the gall-forming rust fungus in Agriculture. CRC, Boca Raton, FL, pp. 33–54. Uromycladium tepperianum (Sacc.) McAlp. to the biological control of Dennill, G.B., Donnelly, D., Stewart, K., Impson, F.A.C., 1999. Insect Acacia saligna (Labill.) Wendl. (Fabaceae) in South Africa. African agents used for the biological control of the Australian Acacia species Entomology Memori 1, 125–128. and Paraserianthes lophantha (Willd.) Nielsen (Fabaceae) in South Myers, J.H., 1978. Selecting a measure of dispersion. Environmental Africa. African Entomology Memori 1, 45–54. Entomology 7, 619–621. Denslow, J.S., Johnson, M.T., 2006. Biological control of tropical weeds: Norambuena, H., Carrillo, R., Neira, M., 1986. Introduccioń, establec- research opportunities in plant-herbivore interactions. Biotropica 38, imiento y potencial de Apion ulicis como antagonista de Ulex 139–142. europaeus en el sur de Chile. Entomophaga 31, 3–10. Freese, A., 1991. Apion hookeri Kirbi (Col., Curculionidae) a potential Norambuena, H., Martıńez, G., Carrillo, R., Neira, M., 2007. Host agent for the biological control of Tripleurospermum perforatum specificity and establishment of Tetranychus lintearius (Acari: Tetr- (Me´rat) Wagenitz [=T. inodorum (L.) C.H. Schultz, Matricaria anychidae) for biological control of gorse, Ulex europaeus (Fabaceae) perforata Me´rat, M. inodora L.] (Asteraceae, Anthemideae) in Canada. in Chile. Biological Control 40, 204–212. Journal of Applied Entomology 112, 76–88. Norambuena, H., Piper, G.L., 2000. Impact of Apion ulicis Forster on Goolsby, J.A., van Klinken, R.D., Palmer, W.A., 2006. Maximising the Ulex europaeus L. seed dispersal. Biological Control 17, 267–271. contribution of native-range studies towards the identification and Picanço, M.C., Barreto, R.W., Fidelis, E.G., Semeao, A.A., Rosado, J.F., prioritisation of weed biocontrol agents. Australian Journal of Moreno, S.C., de Barros, E.C., Silva, G.A., Johnson, M.T., 2005. Entomology 45, 276–286. Biological control of Miconia calvescens by phytophagous arthropods Harris, P., Shorthouse, J.D., 1996. Effectiveness of gall inducers in weed Technical Report 134. Pacific Cooperative Studies Unit, University of Hawaii at Manoa, Honolulu, HI, pp. 31. biological control. Canadian Entomologist 128, 1021–1055. Hill, R.L., Gourlay, A.H., Martin, L., 1991. Seasonal and geographic SAS Institute Inc., 2004. SAS/STAT User’s Guide. Version 9.1. SAS variation in the predation of gorse seed, Ulex europaeus L., by the seed Institute Inc., Cary, NC. weevil Apion ulicis Forst. New Zealand Journal of Zoology 18, 37–43. Scott, J.K., Yeoh, P.B., 2005. Biology and host specificity of Apion Hoddle, M.S., 1991. Lifetable construction for the gorse seed weevil Apion miniatum (Coleoptera: Apionidae) from Israel, a potential biological ulicis (Forster) (Coleoptera: Apionidae) before gorse pod dehiscence, control agent for Emex australis and Emex spinosa (Polygonaceae) in and life history strategies of the weevil. New Zealand Journal of Australia. Biological Control 33, 20–31. Zoology 18, 399–404. Shenefelt, R.D., Marsh, P.M., 1976. Pars 13 Braconidae 9 Doryctinae. In: Hoffmann, J.H., Impson, F.A.C., Moran, V.C., Donnelly, D., 2002. van der Vecht, J., Shenefelt, R.D. (Eds.), Hymenopterorum Catalogus Biological control of invasive golden wattle trees (Acacia pycnantha)by (nova editio). W. Junk, ‘s-Gravenhage, The Hague, The Netherlands, a gall wasp, Trichilogaster sp. (Hymenoptera: Pteromalidae), in South pp. 1265–1267. Africa. Biological Control 25, 64–73. Smith, C.W., 2002. Forest pest biological control in Hawaii, Technical Infante, F., Hanson, P., Wharton, R., 1995. Phytophagy in the genus Report 129. In: Smith, C.W., Denslow, J.S., Hight, S. (Eds.), Monitoriella (Hymenoptera: Braconidae) with description of a new Workshop on biological control of invasive plants in native Hawaiian species. Annals of the Entomological Society of America 88, 406–415. ecosystems. Pacific Cooperative Studies Unit, University of Hawaii at Julien, M.H., Griffiths, M.W., 1998. Biological control of weeds: a world Manoa, Honolulu, HI, pp. 91–102. catalogue of agents and their target weeds. CAB International, Weiss, A.E., Walton, R., Crego, C.L., 1988. Reactive plant tissue sites and Wallingford, UK. the population biology of gall makers. Annual Review of Entomology Kaiser, B.A., 2006. Economic impacts of non-indigenous species: Miconia 33, 467–486. and the Hawaiian economy. Euphytica 148, 135–150. Wharton, R.A., Hanson, P.E., 2005. Biology and evolution of braconid Maceˆdo, M.V.d., Monteiro, R.T., 1989. Seed predation by a braconid gall wasps (Hymenoptera). In: Raman, A., Schaefer, C.W., Withers, wasp, Allorhogas sp. (Hymenoptera). Journal of the New York T.M. (Eds.), Biology, ecology, and evolution of gall-inducing arthro- Entomological Society 97, 359–362. pods. Science Publishers, NH, pp. 495–505.