Control of Brazilian pepper fruit feeding insect Megastigmus transvaalensis (Hymenoptera: Torymidae)

From Biological Control 2001 22: 136-148

G. S. Wheeler (wheelerg@saa.ars.usda.gov)

Abstract. An accidentally introduced torymid wasp, Megastigmus terebinthifolius, originally from South African Rhus spp. was recovered from drupes of Schinus terebinthifolius in Florida. Collections of S. terebinthifolius drupes from 18 sites in Florida during a 2 year period indicated that M. terebinthifolius was present at all sites and this was the only insect that emerged from the drupes. Dissections indicated that the wasp damaged 24% during 1997-1998 and 38.5% of the drupes in 1998-1999. Generally a single generation of wasps occurred each year which was synchronized with the flowering and fruit production period during Nov-Jan. When an additional flowering and fruit production episode occurred, as it did at most sites in Spring 1998, over 75% of the drupes were damaged by the wasp. Germination tests of wasp-damaged drupes indicated that none of the infested monocarpic seeds were viable. Wasps may bridge one season to the next with a diapause which may be broken with a 12 hour photoperiod. Utilization of alternate hosts has not been detected despite rearing of drupes from all the native anacard species within the range of S. terebinthifolius.

Introduction

Brazilian pepper. Schinus terebinthifolius Raddi (Anacardiaceae) is a native of Brazil, Paraguay and Argentina (Ferriter and Clark 1997) and was introduced in Florida and Hawaii as an ornamental shrub and is still sold in many sub-tropical regions around the world (Grissell personal communication). Brazilian pepper is ranked among the most important threats to biodiversity in the south Florida ecosystem (Ewel 1986) and occupies more area in the state than any other invasive species (Schmitz 1994). The species is well known for its copius production of monocarpic, bright red fruits during the Winter. A well known invader of disturbed sites, this species also colonizes several native plant communities including pinelands, hammocks, and mangrove coastal areas of Florida (Ewel et al., 1982). The plant may grow to 10 m in height forming dense monospecific thickets. Not only is the shrub a threat to biodiversity but volatiles produced by the flowers are detrimental to humans as they cause sinus and nasal congestion, headaches, sneezing, eye irritation and labored breathing (Morton 1978). Additionally, ingestion of the berries by birds causes intoxication (Campello and Marsaioli 1974) and the sap from wood causes severe rash and intense discomfort (Morton 1978). The plant is found in southern Florida, southern Arizona, southern Califonia, Hawaii, Puerto Rico and St. John, Virgin Islands (Little et al. 1974). Its distribution in Florida extends from the Florida Keys north to Cedar Key on the west coast and to Daytona Beach on the east coast. The fruit production season of the plant in Florida is from November through February (Ferriter and Clark 1997) and the fruit may remain attached to the tree for several months (Ewel et al. 1982).

Biological control of this species was initiated in Hawaii in the 1950s and has resulted in the release of two caterpillar species, Crasimorpha infuscata (Lepidoptera: Gelechiidae) and Episimus utilis (Lepidoptera: Tortricidae) and a seed feeding beetle Lithraeus atronotatus (Coleoptera: Bruchidae) (Julien 1998). The last two species have established in Hawaii but apparently have had little impact on the target weed populations (Yoshioka and Markin 1991). Similar biological control efforts have been on-going in Florida for over 10 years, and just recently a sawfly Herteroperreyia hubrichi Malaise (Hymenoptera: Pergidae) has been cleared for release in the field (Cuda personal communication).

Surveys of the insect fauna associated with Brazilian pepper have been conducted in Florida and have revealed 115 species, 40% of which were herbivorous (Cassani 1986, Cassani et al. 1989). None of the species are considered promising agents for the reduction of Brazilian pepper populations as none cause significant damage to the plant, most are generalist feeders and many are potential agricultural pests. However, a recent arrival to Florida has appeared that feeds on the seeds of Brazilian pepper. This species, Megastigmus transvaalensis (Hymenoptera: Torymidae) was probably introduced accidentally from Reunion or Mauritius via France in Brazilian pepper fruits sold as spices in exotic food stores (Habeck et al. 1989). This species was also reported from Hawaii (Beardsley 1971) where it was suspected of displacing the biological control agent L. atronotatus (Yoshioka and Markin 1991). Additionally, individuals of the wasp have been collected from the Canary Islands (Grissell 1979), Argentina and Brazil (Grissell unpublished data) and from California (Harper and Lockwood 1961). The host range of this species includes the South American Schinus molle (Hussey 1956; Grissell 1979; Yoshioka and Markin 1991) and four South African Rhus species including R. laevigata, R. verminalis, and R. angustifolia (Grissell, E. E. personal communication). In Florida this species has been reported only from S. terebinthifolius fruits however, considering its purported South African Rhus origin (Grissell unpublished data), this species may constitute a threat to Florida’s native anacards.

The goals of this study include: first, to describe the Florida distribution of M. transvaalensis, the dynamics of their emergence, and their impact on the reproductive output of the plant; second, to determine the impact of wasp damage on seed viability; third, determine the importance of photoperiod as a factor influencing diapause; and finally, to examine the host range of this wasp in Florida from native and non-native members of the Anacardiaceae and other species.

Methods and Materials

Sites and wasp emergence. Collection sites were established throughout the range of Brazilian pepper in Florida. A total of 18 sites were sampled during a two year period (1997-1999). Sites were located from the Everglades National Park northward to Tampa Bay on the west coast, Daytona Beach on the east coast and Orlando in the center of the state (Fig. 1). Samples consisted of 3-4 collections of 100-500 drupes each during the fruit production season. Two collections (Fall & Winter) were made during 1997-1998. Additionally, unexpected flowering and fruiting occurred during the Spring of year 1 (1998) and collections were made in the sites where fresh drupes were present. All drupes were returned to the laboratory where they were reared in a screenhouse under ambient conditions in petri dishes (9 cm) and observed 3 times per week for emergence of wasps. After a period of 2 weeks during which no wasps emerged, the drupes were moved to environmental chambers to test the effect of photoperiod on breaking diapause (see Breaking diapause methods below). The extent of damage by M. transvaalensis feeding was determined by dissecting a subset of the collected drupes (n = 20 with 3 replicates) from each year, season, and site. To determine if there was a seasonal effect on wasp impact, the number of damaged drupes produced during each season was analyzed by ANOVA and the means were compared with a Ryan’s Q mean comparison test (P = 0.05).

During 1998-1999 only a single collection was made at each site as no difference was found in the damage levels between Fall and Winter during year 1 (see Results) and flowering did not occur at any of the sites in the Spring as in year 1. These drupes were brought directly into the laboratory where they were incubated in an environmental chamber 28 ° C; 12:12 photophase:scotophase.

Breaking Diapause. Following the initial emergence period of wasps (at least 2 weeks after which no additional wasps emerged), the drupes were reared in one of 2 treatments. To determine the influence of photoperiod on wasp emergence, the drupes were reared in petri dishes (9 cm) in either a 12:12 h or a 14:10 h photophase : scotophase. Emerging wasps were counted weekly for nearly 140 d and the rate of wasp emergence was analyzed by ANCOVA comparing the regression coefficients of the two photoperiods.

Germination studies. The impact of M. transvaalensis damage to the reproductive potential of S. terebinthifolius was determined by conducting germination tests of mature drupes. Initially the optimal conditions for germination were determined by incubating surface sterilized (10% bleach for 10 min) drupes in petri dishes lined with filter paper moistened with deionized water. Incubation conditions were 20, 25, and 30 ° C in complete darkness for 14 days. An additional treatment included incubation at 25 ° C in a 14:10 h photoperiod : scotophase. Four replicates of 10 drupes each were included. After optimal conditions were determined (See results) paired tests of M. transvaalensis damaged (as indicated by an exit hole) and undamaged drupes were incubated at 20 ° C in complete darkness to determine the impact of wasp feeding on drupe viability. An additional treatment included drupes collected on the ground from small mammal feces, possibly a raccoon. Four replicate incubations of the drupes were conducted of the single feces collection.

Alternate host species. To determine if M. transvaalensis wasps extended their host range to include other plant species, collections were made of drupes from native anacards at several locations and dates throughout the state where these species and S. terebinthifolius were in close proximity (Fig. 1; Table 4). At each of these sites S. terebinthifolius drupes were also collected to determine if the wasp was present. The native anacards included poison ivy (Toxicodendron radicans (L.) Kuntze), poisonwood (Metopium toxiferum (L.) Krug & Urban); and winged sumac (Rhus copallinum L.). Drupes from poison ivy and southern sumac were also collected north of the S. terebinthifolius distribution to determine if the wasp had spread beyond the range of the weed. Additionally, fruits of several non-anacard species and a non-native anacard (e.g., Mangifera indica L., Spondias purpurea L.) were collected to determine if the wasp could feed and complete development in these species.

Results

Sites and wasp emergence. The results of collections made during 1997-1998 indicate that wasps damaged ca. 24% of the drupes during the Fall and Winter and the level of damage increased significantly to over 75% during the Spring (Fig. 2).

Damage estimates from drupes collected during 1998-1999 overall averaged 38.5 %. During both years the percent of drupes damaged at different sites ranged from 1.77% to nearly 100% (Table 1). Of the more than 4000 drupes dissected, only 3 were found to contain live wasps (2 larvae, 1 adult; Fig. 3 and Fig. 4).

During year 1 when collected drupes were reared in ambient temperatures and photoperiod, wasp emergence appeared to approach a plateau after 30 d (Fig. 5). During this period the average temperatures in south Florida were 21.3 ° C (NCDC, NOAA) and the day length ranged from ca. 10.75 h to 11.25 h (http://gears.tucson. ars.ag.gov/beepop/daylight.html). After 48 d the wasps were thought to be in diapause and the drupes were divided between the two photoperiod treatments (see Methods). During year 2 when the drupes were reared under controlled conditions (28 ° C, 12 h photoperiod) wasp emergence continued to increase even 150 d after collection (Fig. 5). Wasps are continuing to emerge from these drupes and the total numbers will be included in the final report. Slightly more females emerged than males, especially in year 1 where the ratio was 68.1 : 31.9 and in year 2 it was 57.1 : 42.9. Typically when the drupes were collected early (e.g., November) the males were found emerging 1-2 d prior to the females. No other insect species emerged from S. terebinthifolius drupes.

Breaking Diapause. Exposure of S. terebinthifolius drupes to different photoperiods influenced the cumulative emergence of M. transvaalensis wasps. Wasps emerged more rapidly from drupes in the 12 h photoperiod compared with those incubated in the 14 h photoperiod (Fig. 6). Rearing of drupes terminated after 140 d and by this time 189 and 144 wasps had emerged from the 12 h and the 14 h treatments, respectively.

Germination studies. Preliminary tests indicated that drupe germination was significantly affected by both light and temperature. Drupes exposed to light at 25 ° C had significantly lower percent germination compared with the other treatments. The best conditions found were in darkness at 20 ° C, where 90% of the drupes germinated (Table 2).

Drupes collected from animal feces incubated at 20 ° C in darkness had significantly greater percent germination compared to either the intact or the wasp-damaged drupes (Table 3). Additionally, none of the wasp-damaged drupes germinated, compared with ca. 46% of the intact drupes.

Alternate host species. Multiple collections were made of all the native members of the Anacardiaceae of south Florida and one non-native species of the family, Spondias purpurea (Table 4). These native anacard species included those species whose distribution overlapped that of S. terebinthifolius, namely poison ivy (Toxicodendron radicans), poisonwood (Metopium toxiferum), and winged sumac (Rhus copallinum). No insects have emerged from any of these collections, however most collections are relatively recent (March-April 1999). Wasps have emerged from the Ft Myers and the Navy Wells (Dade Co.) collections of S. terebinthifolius drupes made at the same time as the other anacard species collections. These results indicate that wasps were present and presumably had the opportunity to utilize other host species. These and other sites where native anacards are present in south Florida are being monitored monthly and collections of mature fruit will be made when available.

Several species that produce similar size or shape berries were collected. Two similar species of chalcidoid wasps Megastigmus floridanus Milliron and Torymus rugglesi Milliron were reared from fruit of dahoon holly, Ilex cassine collected at Mahogany Hammock (ENP). This is the first report of these species feeding on this host (Grissell 1989). We will continue to monitor all collected fruit and report the findings in the final version of this document.

Discussion

Damage by natural populations of the South African wasp M. transvaalensis significantly reduced S. terebinthifolius seed viability. The wasp is widely distributed throughout the range of S. terebinthifolius in Florida and was recovered from all sites visited causing seed mortality from less than 2 to nearly 100%. Overall, during the two years of this study, seed mortality from wasp damage averaged 25-38.5% during the primary fruit production period (Nov – Jan). In years or populations (ca. 10%; Ewel et al. 1982) that have an additional fruit production period, as in the Spring in 1997-1998, much higher seed mortality may occur (75%). These damage levels are considerably higher than those reported in Hawaii where they were reported to damage almost 10% of the seeds in 1988 (Yoshioka and Markin 1991). Moreover, they exceed the estimates made for Florida populations (< 5%) based only upon wasp emergence not fruit dissections (Habeck et al. 1994). As S. terebinthifolius reproduces primarily by seed production, our results suggest that the wasp has a significant impact on the spread of the weed. Coupled with the reportedly low seedling survival especially in mature communities (50%; Ewel 1986), these results suggest that wasp damage significantly contributes to reducing the spread of this weed species, impeding the invasion into natural areas, and the displacement of native species.

The wasp appears to typically have a single generation per year, entirely dependent upon the synchronous flower and fruit production period of its host, S. terebinthifolius. The lack of an increase in the rate of wasp damage between the Fall and Winter collections suggest only a single wasp generation. The exception to this may be the atypical Spring fruit production period observed during the 1998 season where increased levels of damage were found. Although the level of damage was greater during 1998-1999 it did not achieve the same level as that during Spring 1998 suggesting high mortality between flowering seasons. This may be a common restriction of the wasp’s life cycle as indicated by only 3 live wasps found from the over 4000 drupes dissected. Possibly this is a sufficient number of overwintering individual to bridge one year to the next. Moreover, we did not find any evidence to suggest that the wasps were developing on alternate hosts.

When drupes were reared under ambient photoperiod and temperature wasp emergence appeared to reach a plateau after 30d, suggesting either most of the wasps had emerged or the wasps were delaying emergence pending a required environmental cue. This cue may have been the 12 h photoperiod as emergence increased in drupes reared under these conditions compared with those reared in 14 h conditions. This 12 h daylength is similar to that found during Fall just prior to S. terebinthifolius flowering in southern Florida. Other species of Megastigmus are also known to remain inside host seeds for extended periods of 1 – 2 years (Milliron 1949) and may be a common phenomenon of this group.

As the wasp originates from South African Rhus spp. it would not be surprising to find this species feeding on Florida’s native Rhus or other anacard species. In Florida M. transvaalensis wasps have been reared only from S. terebinthifolius fruits. Presently we are monitoring numerous collections made from several species for wasp emergence. We will continue collecting mature fruits of the native anacards as they become available. Surveys have been conducted in Florida of the herbivores associated with poison ivy Toxicodendron radicans but no mention was made of fruit-feeding species (Habeck 1990). Even though several of these anacard species may be undesirable to humans, the fruit and leaves are important food for native species of birds and small mammals (Martin et al. 1951). If this wasp successfully utilizes other native species and threatens the stability of their populations the value of this species as a S. terebinthifolius control agent will be controversial. However, we have yet to find evidence of any host extension in Florida. In fact, this species has never been reared from anything in the U.S. other than exotic Schinus spp.

Acknowledgements. We are indebted to the technical assistance of Mark Endries, Ben Montgomery, Tracy Davern, Jamie Zahnizer, and Lisa Massey, AmeriCorps, Students Conservation Association. Dr. W. Mashaka assisted in collections made in Everglades National Park. Collections were made with the cooperation of Florida Dept of Environmental Protection (Permit # 1065); Miami-Dade Co. Parks (Permit # 0007) and the Everglades National Park (Permits # 19970114 & 19990011). Insect identifications were generously provided by Dr. E. E. Grissell, Systematic Entomology Laboratory, National Museum of Natural History, Washington, DC. Voucher specimens were deposited at the National Museum of Natural History. Financial support was provided by Florida Dept of Environmental Protection.

References cited