Proc. Fla. State Hort. Soc. 121:363–369. 2008.
Erythrina Gall Wasp, Quadrastichus erythrinae (Hymenoptera: Eulophidae) in Florida, and Susceptibility of Erythrina herbacea (Fabaceae)
FORREST W. HOWARD1*, ROBERT W. PEMBERTON2, AND HONG LIU3 1University of Florida, IFAS, Fort Lauderdale Research & Education Center (FLREC), 3205 College Avenue, Fort Lauderdale, FL 33314 2United States Department of Agriculture, Agricultural Research Service, Invasive Plant Laboratory, 3225 College Avenue, Fort Lauderdale, FL 33314 3Florida International University, 11200 SW 8th Street, Miami, FL 33199
ADDITIONAL INDEX WORDS. Quadrastichus erythrinae, invasive insect pests, coral-bean, native plants Erythrina gall wasp (EGW), Quadrastichus erythrinae Kim, and the extent of its galling and associated damage to Ery- thrina spp. hosts were observed in a research nursery and in natural and landscaped areas in southern Florida. In the research nursery, galling and resultant damage to Erythrina herbacea L., a native plant, were highly variable on four dates during a 1-year period. On one examination date, when the susceptibility levels of three species of Erythrina were compared, there was a higher mean percentage of galled leaves on Erythrina variegata L. than on Erythrina herbacea, and minimal galling on Erythrina humeana Sprengel. Based on several criteria, E. variegata was the most susceptible of these hosts. Preliminary field observations on the behavior of EGW are reported. Erythrina amazonica Krukoff is reported as a new host of EGW.
Fig. 1. Erythrina gall wasp, Quadrastichus erythrinae, adult.
The erythrina gall wasp (EGW), Quadrastichus erythrinae Kim (Fig. 1), attacks various species of Erythrina by oviposit- ing in the plant tissue, where the larvae develop and induce the formation of galls in leaves, petioles and tender stems (Fig. Erythrina variegata 2a–d). It was described as a new species in 2004 and since then Fig. 2a. Laminar galls of erythrina gall wasp on . has been reported in many tropical and warm climate localities, including American Samoa, China (Guangdong Province, Hong a specimen collected on 15 Oct. 2006 at the Metro Zoo in Miami- Kong), Guam, India, Japan (Okinawa Prefecture), Mauritius, Dade County, FL, by Edward Putland and Olga Garcia [Florida Philippines, Singapore, Taiwan, Thailand, Hawaii, and Florida, Department of Agriculture, Division of Plant Industry (DPI)] on USA (Uechi et al., 2007; Wiley and Skelley, 2006; Yang et al., Erythrina variegata L. (Wiley and Skelley, 2006). As of 24 June 2004). The first Florida and Continental US record was based on 2008, EGW had been found in Florida in the following counties: Miami-Dade, Broward, Palm Beach, St. Lucie, and Indian River on the East Coast and Collier, Lee, and Charlotte on the west Acknowledgments. We thank Bryan Steinberg and Sergio Gallo of the FLREC staff coast (James Wiley, DPI, personal communication). The insect for assistance in field work. We also thank the following personnel of the Florida is considered a new introduction in all of the localities where Department of Agriculture and Consumer Services, Division of Plant Industry: it has been discovered, and its native home is presumed to be James Wiley for verifying identifications of EGW and providing distribution records of this insect in Florida; Richard E. Weaver and Patty J. Anderson for somewhere in Africa (Wiley and Skelley, 2006). In the localities verifying identifications of Erythrina spp. where it has been introduced, it has spread quickly and its impact *Corresponding author; email: fwhoward@ufl.edu on erythrina trees has been severe. For example, in Hawaii, the
Proc. Fla. State Hort. Soc. 121: 2008. 363 first record of this wasp was in 2005 on Oahu; within 6 months it had spread to the remaining main islands of Hawaii and has caused severe galling of thousands of exotic erythrina species grown as ornamentals, and of the endemic E. sandwicensis Degener in natural areas (Gramling, 2005; Heu et al., 2005). A parasitoid wasp collected in Africa is under study for possible release as a biological control agent of EGW in Hawaii (Gates and Delvare, 2008). In Nov. 2006, we observed galls typical of this wasp on a single tree of Erythrina variegata L. on the grounds of the Fort Lauderdale Research and Education Center (FLREC), which is about 70 km from the Metro Zoo. Specimens of gall wasps were reared from the galls and identified as E. erythrinae by James Wiley, Florida State Collection of Arthropods (DPI Specimen No. E 2007-1755-1). The genus Erythrina contains more than 100 species that are distributed throughout the tropics and warm regions of the Fig. 2b. Petiole gall of erythrina gall wasp on Erythrina herbacea. world (Kass, 1994; Bruneau, 1996; Staples and Herbst, 2005). All known hosts of the EGW are species of Erythrina that were growing in localities invaded by the EGW. Prior to finding the EGW in Florida, these included Erythrina variegata L., E. coral- lodendron L., E. crista-galli L., E. abyssinica DC, E. berteroana Urban, E. sandwicensis Degener, and E. fusca Laur. (Li et al. 2006). (The more widely cultivated species of Erythrina are known by different vernacular names in different localities, and the same or a similar vernacular name, often including the words “coral tree,” “coral-bean,” etc., may be applied to multiple species. Thus, for clarity, species of this genus will be referred to in this report by their scientific names.) There are four exotic Erythrina spp. in a checklist of the woody cultivated plants of Florida (Burch et al., 1988), but erythrina trees are relatively infrequent in the urban landscape of southern Florida. They are more important as ornamentals in various other localities. Several species are highly important in agroforestry in tropical areas (Kass, 1994). Erythrina herbacea L. (Fig. 3a–d), the only species of the genus native to Florida, occurs naturally as a shrub or small tree
Fig. 2c. Stem gall of erythrina gall wasp on Erythrina herbacea.
Fig. 2d. Inflorescence of Erythrina variegata galled by erythrina gall wasp. Fig. 3a. Erythrina herbacea, inflorescences.
364 Proc. Fla. State Hort. Soc. 121: 2008. Fig. 3d. Erythrina herbacea, seedpods. Fig. 3b. Erythrina herbacea, trifoliate compound leaf.
Materials and Methods
OBSERVATIONS ON ERYTHRINA GALL WASP AND ITS DAMAGE. To verify the association of EGW with the galls found on Erythrina hosts, the galls were dissected to verify that EGW larvae and pupae were present (Fig. 4). EGW galls were examined to determine their form on different plant parts, and the numbers of galls per leaf. Dimensions of laminar and petiole galls on different species of Erythrina were measured with calipers. Adult wasp activity was observed. Yellow sticky traps 7.5 × 13 cm (3 × 5 inches)(Olson Products, Medina, OH) were placed on plants or other objects for varying periods to compare numbers of adult wasps in the vicinity of galled vs. gall-free erythrina plants and at distances
Fig. 3c. Erythrina herbacea, foliage. on the coastal plains from North Carolina through Florida and along the Gulf Coast to Tamaulipas, Mexico (Wunderlin and Hansen, 2008). It is an important component of the understory in natural forests (e.g., it is a nectar source for hummingbirds), and is planted as an ornamental in urban areas within its natural range. We are thus particularly concerned about the potential impact of the EGW on this plant species. This paper reports on 1) some preliminary field observations of the activity of EGW and appearance of and damage by its galls, and 2) the results of a field trial to determine the susceptibility of the native E. herbacea to galling by this wasp compared to galling on several Erythrina spp. that are grown in Florida as Fig. 4. Erythrina gall wasp, Quadrastichus erythrinae, pupa shown in dissected exotic ornamentals. gall on Erythrina variegata.
Proc. Fla. State Hort. Soc. 121: 2008. 365 of several meters from erythrina plants. An experiment was con- in many cases were coalesced so as to appear as one extensive ducted during 6 d in May 2007 to compare day and night activity lumpy swelling. of EGW adults: a sticky trap was placed on a 0.7-m- (2.3 ft) tall In addition to verifying the initial identification of EGW at containerized highly galled E. variegata at 0600 HR. At 1800 HR, the FLREC on E. variegata as noted above, Mr. Wiley also veri- the trap was removed for examination under the microscope to fied the identification of EGW on E. herbacea test plants (DPI determine the number of EGWs, and a fresh trap was attached to Specimen No. E 2007-2950-1). This is a new Florida host record the plant and traps changed again at 0600 HR the next day. This for Q. erythrinae. We examined 10 randomly selected galled procedure was repeated for 6 days and nights. leaflets on 1 July 2008 on E. herbacea and the same number on Field trial on susceptibility of Erythrina spp to EGW. Container- leaflets of E. variegata. There was a mean of 3.6 (SD=3.5, range ized plants in 11.4-L (3 gal) containers were obtained in Mar. and 1–10) galls per leaflet on E. herbacea and 26.4 (SD=12.7, range Apr. 2007 from local commercial nurseries. The species included 10-49 galls per leaflet), on E. variegata. The mean diameters of E. variegata, E. herbacea, E. humeana Sprengel, and E. verna laminar galls were 4.3 mm (SD=0.9) on E. herbacea and of 4.6 Vell., (syn., E. mulungu Benth.). Except for sparse EGW galling (SD=0.5) on E. variegata. on E. variegata, the plants were not galled when purchased. Ac- Petiole galls (Fig. 2b) were formed on different portions of cording to nursery personnel, none of the plants had been treated the petiole, often in the pulvinus. Measurements of galls made with insecticides. We were particularly interested in E. herbacea, on 1 July 2008 are reported as follows: The mean diameter just a native plant. According to the nursery owner, about 80% of the above the pulvinus of 10 randomly selected gall-free petioles test plants of this species had been propagated from seeds rather was 1.3 mm (SD=0.17) in E. herbacea and 2.4 mm (SD=0.48) than cuttings. Thus, they were highly diverse genetically. in E. variegata. The mean diameter of galled pulvini was 2.6 The containerized plants were placed in a research nursery mm (SD=0.45) and 4.3 mm (SD=0.79) in E. herbacea and E. at the FLREC. This nursery is about 300 m from the arboretum variegata, respectively. The mean diameter of petiole galls on where EGW was first identified at the FLREC. To provide hosts petioles above the pulvini was 3.8 mm (SD=0.90) and 6.5 mm to support field populations of EGW near the nursery, additional (SD=1.51)in E. herbacea and E. variegata, respectively. These plants of E. variegata were propagated by cuttings and were results were consistent with observations in India that petiole grown either in containers in the nursery or planted in the field galls of EGW appear as portions of petioles swollen about 3× about 20 m from the nursery. The test plants were maintained their normal thickness (Faizal et al., 2006). The mean lengths of under 50% shade cloth, fertilized about every 3 months with 15 petiole galls was 8.64 mm(SD=3.27) and 18.4 mm(SD= 7.61) in mL (1 tbsp) per plant of Osmocote (17N–6P–9K) and irrigated E. herbacea and E. variegata, respectively. with 3 cm (1.2 inches) of water on alternate days by overhead The larger size of both laminar and petiole galls on E. var- sprinklers, except during rainy periods. Twenty E. herbacea plants iegata compared to E. herbacea is compatible with our general were placed in a single group, with plants of other Erythrina spp. observation that E. variegata tended to be more highly galled placed adjacently, including five E. humeana, eight E. variegata, than E. herbacea, and the galls on the E. variegata tended to and one E. verna. The presence of EGW in the vicinity was oc- be larger. Whether larger galls produce larger numbers of EGW casionally checked by placing a yellow sticky trap on a plant or adults remains unknown. nearby post for several hours. Highly galled leaves shriveled and eventually desiccated and On four examination dates (3 July and 14 Sept. 2007; 1 May were shed, causing severe defoliation of some hosts. This was and 27 June 2008) the E. herbacea plants were examined for especially frequent in E. variegata (Fig. 5). When the defoliated galls of EGW. To obtain data on the susceptibility of this species trees flushed new leaves, these were soon galled. After repeated to galling by EGW, we determined on each plant 1) the number galling, small E. variegata trees died within months, but at least of leaves with at least one laminar gall, 2) the number of leaves with at least one petiole gall, and 3) the number of leaves per plant. With these data we calculated for the E. herbacea test plants the percentage of leaves with laminar galls per plant and the percentage with petiole galls per plant. We also determined the numbers of stem galls per plant, and the mean heights of the test plants of each species. On the 1 May 2008 examination date, in addition to the obser- vations of E. herbacea as described, similar observations were made of galling of several each of E. humeana and E. variegata and on one E. verna. Also, we have included observations on EGW on Erythrina spp. in several locations.
Results and Discussion
OBSERVATIONS ON ERYTHRINA GALL WASP AND ITS DAMAGE. The EGW galls occurred on leaf laminae, petioles, and tender stems of susceptible Erythrina spp., and larvae and pupae of the EGW were readily found by dissecting galls (Fig. 4). Galls that occurred on leaf laminae usually developed on the adaxial (upper) surface as dome-shaped galls with open hollows on the abaxial (lower) Fig. 5. Stem of Erythrina variegata severely galled by erythrina gall wasp, with surface. The laminar galls usually occurred in groups, which resulting defoliation.
366 Proc. Fla. State Hort. Soc. 121: 2008. were consistently skewed toward males, as has been reported by (Faizal et al., 2006). In the sticky trap experiment to compare day and night trap catches during 6 days and nights there was a mean of 17.5 male and 13.3 female EGWs captured per day during daylight hours. None were caught at night. This indicates that adult EGW flight activity is diurnal.
Experiment and observations on susceptibility of Erythrina spp. to EGW In E. herbacea, the percent of the leaves with petiole, laminar, and stem galls varied on the four different examination dates (Table 1), being minimal on the 1 May 2008 observation date, and peaked on the 3 July 2007 observation date. Observations on 27 June 2008 showed a substantial increase from the previous month, but a low level compared to those of the previous year. Erythrina herbacea is characterized as persistent to semi- Fig. 6. A large tree, Erythrina variegata, in Fort Lauderdale, FL, surviving after deciduous (Gilman, 2007), but possibly this species may retain more than a year under attack by erythrina gall wasp. Galls are abundant but not highly noticeable from a distance. a greater portion of its winter foliage in southern Florida than in more northern areas of its range. We obtained no data on the seasonal incidence of leaf abscission in E. herbacea, but noted one large tree of this species survived galling that was first observed that the plants bore foliage year-round. Thus, unlike Erythrina the previous year (Fig. 6). This tree is presently (July 2008) galled, spp. that are fully deciduous, E. herbacea could harbor EGW however, and the potential long-term effect of repeated galling populations continuously. of a tree by EGW may be lethal (Yang et al., 2004). On the 1 May 2008 observation date, when galling was com- The presence of EGW in each of the countries where it has pared on three species of Erythrina (Table 2), E. variegata had thus far been reported was initially detected by finding exten- the highest percentage of leaves infested with laminar galls, i.e., sively galled plants and rearing the wasps from the galls. By 30.0% (SD=11.37). This species has been previously reported as that phase of its invasion, EGW is probably well dispersed in highly susceptible to EGW (Heu et al., 2005; Yang et al., 2004). its new locality. Yellow sticky traps capture EGW (Smith et al., In the five E. humeana plants, there was one full laminar gall 2007) (Fig. 7), but based on our observations they may be of on one plant, and a mean of 9.7% (SD=10.2) of the leaves had limited value in early detection of this species. For example, in procecidial growths (i.e., evidence of an initiation of a plant gall Mar. 2007, a yellow sticky trap was placed 2 m high in a heavily that did not develop). One small E. verna Vell. Conc. (Syn. E. galled E. variegata, upon which numerous EGW were crawl- mulunga Martius) [height, 0.50 m (1.6 ft)], a species native to ing and making short flights. A similar trap was placed at the South America, was adjacent to the test plants during the 14-month same height in a frangipani tree, Plumeria alba L., at 8 m (26.2 EGW exposure period. It remained free of galls when examined ft) distance. Three days later, the trap in the erythrina tree had in July 2008. As noted above, the percentage of galled leaves and caught 929 male and 110 female EGW. During the same time galled petioles on E. herbacea was minimal on this date (Tables period, the trap at 8 m distance caught only two female EGW. 1 and 2), but on other observation dates the incidence of galling Similarly, sticky traps placed on highly galled erythrina trees of E. herbacea was much higher. captured large numbers of EGW, while traps on nearby gall-free EGW galls did not fully develop on any of five Erythrina hu- erythrina trees or wooden posts caught few to none. Apparently, meana, a species of African origin. Further testing could perhaps yellow sticky traps are not attractive to EGW, at least not over a confirm that this species is resistant to EGW. distance, but act only as “blunder” traps so that large numbers are Although EGW galling on Erythrina herbacea varied consid- caught if the traps are placed where populations of the insect are erably on different dates, in no case did the percentage of galled concentrated, i.e., in highly galled trees. Trap catches of EGW leaves reach the maximum levels seen on E. variegata nor did plants die. The long-range effects of galling on plant vigor might be significant, however. Based on our observations, the incidence of galling by EGW fluctuates considerably throughout the year. It may be influenced by a complex interplay of factors, including the rate of leaf pro- duction, natural abscission, leaf shedding due to severe galling, and various weather factors, all of which should be considered in any future attempts to evaluate Erythrina spp. for susceptibil- ity to EGW. It will be particularly important that observations be repeated over time. Our method of comparing species by the percent of galled leaves seems adequate for determining their relative susceptibility. However, this method did not generate data on the number of galls per unit area of leaf, which is an important Fig. 7. Yellow sticky traps used to monitor erythrina gall wasps (minute dark consideration in measuring susceptibility. objects; meandering lines were drawn by observer to aid counting), showing Observations elsewhere than the FLREC revealed that EGW (left to right) large, moderate, and small numbers of wasps trapped. has invaded and caused plant damage on some sites and not on
Proc. Fla. State Hort. Soc. 121: 2008. 367 Table 1. Observations on galling by erythrina gall wasp on 20 plants of Erythrina herbacea on four dates, 2007–08, Fort Lauderdale, FL. Date of Mean ht (cm) and SD Mean no. and SD Mean percent and SD Mean percent and SD Mean no. stem observations of test plants. of leaves per plant of leaves with laminar galls. of leaves with petiole galls galls per plant. 3 July 2007 61.4 (SD=19.3) 56.7 (SD=37.3) 13.08 (SD=14.8) 8.27 (SD=11.4) 2.9 (SD=4.1) 14 Sept. 2007 90.8 (SD=21.2) 159.7 (SD=67.1) 0.21 (SD=0.6) 0.24 (SD=0.6) 0.60 (SD=0.9) 1 May2008 120.0 (SD=28.0) 67.7 (SD=43.2) 0 0.49 (SD=1.5) 0 27 June 2008 119.8 (SD=26.7) 149.7 (SD=98.6) 1.0 (SD=1.8) 8.64 (SD=8.8) 1.75 (SD=3.1)
Table 2. Comparison of susceptibility to erythrina gall wasp of three species of Erythrina based on the percent of leaves galled per plant. Observa- tions on 1 May 2008 at Fort Lauderdale, FL. Species of Mean leaves Mean percent of leaves Mean percent of leaves Erythrina No. of test plants Mean ht (cm)z per plantz with leaf gallsz with petiole gallsz variegata 7 84 (SD=54) 21.2 (SD=13.3) 30.0 (SD=11.4) 15.0 (15.98) humeana 5 98 (SD=38) 28.8 (SD=12.4) —y 0 herbacea 20 120 (SD=28) 67.6 (SD=43.2) 0 0.49 (1.51) zMeans followed by standard deviation in parenthesis. yOne fully formed gall on one plant, and mean of 9.7 procecidial growths per plant on 5 plants. others. In a natural area in Kendall Indian Hammocks Park, Mi- ami, the second and third authors observed EGW galls in Nov. 2006, at which time three of 15 E. herbacea plants were galled. In the infested plants, the mean percent of galled leaves was 14.4 (SD=7.6). However, no wasps emerged from collected galls. When this site was visited in May 2007, no galls were found on E. herbacea. Five additional E. herbacea distributed in two dif- ferent natural areas in Broward County were examined in May 2007 and found to be free of galls. On an urban landscape site in Lee Co, in June 2008, E. herbacea had up to 15 galls per leaflet (Fig. 8) (Stephen H. Brown, UF/IFAS, Lee Co. Coop. Ext. Serv., Personal communications). The small E. variegata tree on which EGW galls were first observed at the FLREC had been propagated from a cutting from a mature tree, about 38 cm (15 inches) in dbh, on private property in Fort Lauderdale. When examined in Mar. 2007 the mature tree was extensively galled by EGW. By Summer 2007 it was Fig. 8. Erythrina herbacea with high level of galling by erythrina gall wasp, largely defoliated, and remained so until early Spring 2008, when Lee County, FL. Photo courtesy of Stephen Brown, Lee County Cooperative it flushed new leaves. As of June 2008, this tree has refoliated, Extension Service. and galls are present, but not highly noticeable from a distance (Fig. 6). According to the property owner, no chemical treatment had been applied to the tree. Apparently this tree had sufficient Testing of E. verna, which our preliminary observations indicate reserves to survive the first, and thus far the second, attack of might be resistant to EGW, should be expanded. Additional re- EGW, but repeated attacks may prove more destructive. search on the potential susceptibility to EGW of Erythrina spp. In contrast, the small tree, about 5 cm (2 inches) in dbh, and native to the Americas should be conducted. 1.5 m (4.9 ft) tall propagated from the mature tree noted above died in Summer 2007 after becoming extensively galled, as did Literature Cited many other small erythrina trees at the FLREC. This suggests Bruneau, A. 1996. Phylogenetic and biogeographical patterns in Eryth- large trees may have reserves that enable them to survive initial rina (Leguminosae: Phaseoleae) as inferred from morphological and attacks better than small trees, especially if planted too recently chloroplast DNA characters. Systematic Bot. 21:587–605. to have become well established. However, observations else- Burch, D., D.B. Ward, and D.W. Hall. 1988. Checklist of the woody where indicate that EGW attacks on large trees may be lethal cultivated plants of Florida. Ext. Sale Publ. SP-33, IFAS, University if several successive flushes of foliage are lost due to galling of Florida, Gainesville. (Yang et al., 2004). Faizal, M.H., K.D. Prathapan, K.N. Anith, C.A. Mary, M. Lekha, and There are about 70 species of Erythrina in tropical America C.R. Rini. 2006. Erythrina gall wasp, Quadrastichus erythrinae, yet (Kass, 1994). During a visit in Nov. 2006 to Fairchild Tropical another invasive pest new to India. Curr. Sci. 90:1061–1062. Botanic Garden, Erythrina amazonica Krukoff was found to be Gates, M. and G. Delvare. 2008. A new species of Eurytoma attacking galled, and EGW was reared from the galls. This species has not Quadrastichus spp. (Hymenoptera: Eulophidae) galling Erythrina spp. with a summary of African Eurytoma biology and a checklist. been previously reported as a host of EGW. Zootaxa 1751:1–24. Erythrina corallodendron, which is native to the Greater Gilman, E.F. 2007. Erythrina herbacea. Coral bean, cardinal spear. Antilles, and E. berteroana, native to Central America, have been
368 Proc. Fla. State Hort. Soc. 121: 2008. sting of foreign wasps. Science 16:1759–1760. Staples and D.R. Herbst (eds.). A tropical garden flora. Bishop Museum Heu, R.A., D.M. Tsuda, W.T. Nagamine, J.A. Yalemar, and T.H. Suh. Press, Honolulu. 2005. Erythrina gall wasp, Quadrastichus erythrinae Kim. University Uechi, N., T. Uesato, and J. Yukaway. 2007. Detection of an invasive of Hawaii, Manoa. gall-inducing pest, Quadrastichus erythrinae (Hymenoptera: Eulophi- Kass, D.L. 1994. Erythrina species—Pantropical multipurpose tree dae), causing damage to Erythrina variegata L. (Fabaceae) in Okinawa legumes, p. 404. In: R. Gutteridge and M. Shelton (eds.). Forage tree Prefecture, Japan. Entomol. Sci. 10:209–212. legumes in tropical agriculture. CAB Intl., Wallingford, UK. Wiley, J. and P. Skelley. 2006. Erythrina gall wasp, Quadrastichus Li, H.-m., H. Xiao, H. Peng, H.-x. Han, and D.-y. Xue. 2006. Potential erythrinae Kim, in FDACS, DPI, Gainesville, FL. global range expansion of a new invasive species, the erythrina gall Wunderlin, R. and B. Hansen. 2008. Atlas of Florida vascular plants. wasp, Quadrastichus erythrinae Kim (Insecta: Hymenoptera: Eulo- Consulted Nov. 2008.
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