The influence of turfgrass genotype (bermudagrass, Cynodon dactylon (L.), centipedegrass Eremochloa ophiuroides Munro Hack, St. Augustinegrass Stenotaphrum secundatum [Walt.] Kuntze, zoysiagrass, Zoysia spp., and tall fescue, Festuca arundinacea Schreb) on occurrence of hymenopteran parasitoids was evaluated in residential turf during May, June and July in 2005. Most wasps belonged to Chalcidoidea (55%) and Platygastroidea (29%). Adult wasps representing Mymaridae, Platygastridae, Scelionidae and Braconidae were captured in all turfgrasses. Among all wasps, 26.5% were mymarids and included Gonatocerus sp. and Mymar sp. Eulophidae, Aprostocetus and Pnigalio sp. were less abundant in centipedegrass compared with other turfgrasses. Trichogrammatids (18.2% of total wasps) were more abundant in St. Augustinegrass or tall fescue than in zoysiagrass. Platygastrid wasps, Allotropa and Fidiobia sp., were most often collected from zoysiagrass and St. Augustinegrass. Scelionids represented 23% of the total parasitoids collected. Baeus sp., a scelionid, was found in all turf types except in tall fescue, whereas another scelionid, Trimorus sp., was found among all turfgrass taxa. Figitids were most common in St. Augustinegrass, whereas a greater number of dryinid wasps were found in tall fescue than in all other turfgrasses. Vacuum sampling proved to be a better collecting technique than sweep netting for minute wasps. Chalcidoidea, particularly mymarids, eulophids and trichogrammatids, were abundant in July. Most aphelinid wasps were captured in June with none collected in July. Ichneumonids and braconids were more common in June than in July. Knowledge of species occurrence, abundance and distribution is important for conservation as well as pest management efforts. Our results demonstrate an abundant and diverse community of parasitic wasps in residential turfgrasses in central Georgia that could be a focus of conservation efforts.
Natural enemy communities may be shaped temporally or spatially by direct natural enemy-prey or indirect host plant-prey interaction (Price 1986). Host plants have been shown to influence parasitism, e.g., parasitism of forest caterpillars (Lill et al. 2002), suggesting the possibility of top down influence on host plant use. In the turfgrass environment, studies have revealed a range of herbivore-turfgrass genotype interaction effects (e.g., Braman et al. 1994, 2000a, b, Joseph and Braman 2009a, Reinert and Vinson 2010). Marked effects of individual plant taxa and landscape complexity on natural enemies associated with turfgrass also have been demonstrated (Braman et al. 2002, 2003, 2004, Frank and Shrewsbury 2004, Joseph and Braman 2009b). Evaluation of hymenopteran parasitoids in the turfgrass ecosystem has largely focused on key pests, e.g., Japanese beetle, Popillia japonica Newman (Cappaert and Smitley 2002, Rogers and Potter 2002), southern chinch bug, Blissus insularis Barbar (Reinert 1972, 1978), rhodesgrass scale, Antonina graminis Maskell (Chantos et al. 2009, Dean and Schuster 1958, Dean et al. 1961, Questel and Genung 1957, Riherd 1950, 1951), and mole crickets, Scapteriscus spp. (Hudson et al. 1988, Held 2005, Abraham et al. 2010) on golf course and landscape turf. Other studies reported parasitism by braconid wasps on fall armyworm, Spodoptera frujiperda (J. E. Smith) (Ashley et al. 1983, Braman et al. 2004) and dryinid wasps parasitizing leaf and planthoppers on forage-type bermudagrass (Buntin 1989).
Broader surveys of parasitic Hymenoptera in turf are less well represented. Families of parasitoids captured on sticky traps in buffalograss (Heng-Moss et al. 1998) included Scelionidae, Encyrtidae, Mymaridae, and Trichogrammatidae. Mymarids and trichogrammatids were the most abundant parasitoid families in that study, representing 76.8% of the total parasitoids collected. In a subsequent study scelionid wasps represented 66.3% of the total parasitoids collected in buffalograss (Carstens et al. 2007).
Knowledge of species occurrence, abundance and distribution is central to conservation as well as pest management efforts. Residential and recreational turfgrass sites are often under intensive management, with regular mowing and fertilization, and often pesticide applications (Braman et al. 1997, Carstens et al. 2007) all of which may impact parasitoid dynamics. Wang et al. (2001), for example, reported that a lower density of scelionids was found in chlorpyrifos-treated bermudagrass than in untreated bermudagrass. A better understanding of resident parasitic hymenopterans and how they are influenced by turfgrass taxa will improve conservation efforts based on knowledge of ecosystem dynamics.
Materials and Methods
Twenty-one urban lawns in Spalding Co., GA, were sampled during May, June and July in 2005. A preliminary questionnaire indicated that none of the lawns were treated with insecticides within a 12-month period prior to sampling. Sites included 2 common bermudagrass (Cynodon dactylon (L.)), 9 centipedegrass (Eremochloa ophiuroides Munro Hack), 6 St. Augustinegrass (Stenotaphrum secundatum [Walt.] Kuntze), 3 zoysiagrass, (Zoysia spp.), and 1 tall fescue, (Festuca arundinacea Schreb.) lawns.
Two methods, sweep netting and vacuum suctions, were used to sample parasitic wasps. Samples were collected from a 9.1 × 9.1-m transect from each residential lawn. This area was further subdivided into quadrants (plots) of 4.6 × 4.6 m. Twenty-five sweeps were collected along a diagonal in each quadrant and were stored in plastic bags. The sweep net (Ward's Rochester, NY) had an opening of 0.03 m2 area, net volume of 0.024 m3, and handle-length of 0.92 m. Twenty random suctions of 0.4 m2 lawn area using a ‘Vortis’ vacuum sampler (Burkhard Manufacturing Co., Ltd, Herefordshire, England) were collected . The air throughput of the vacuum sampler was 10.5 m3 per min. Both types of samples were temporarily stored overnight at 4°C, then cleaned using 0.84 mm and 3 mm mesh sieves and permanently stored in 70% ethanol for subsequent evaluation. Parasitic wasps were identified to family or genus using a stereomicroscope (10 × magnification). Hymenopterans were identified to genus by taxonomists at the Systematic Entomology Laboratory, Agricultural Research Service, US Department of Agriculture, Beltsville, MD.
Abundance data for parasitic wasps were analyzed for effect of turfgrass taxon, sampling method and date. ANOVAs were conducted using the GLM procedure of SAS (SAS Institute 2003). Number of wasps collected was the response variable. Differences in least square means were determined by pairwise t-tests.
Results and Discussion
We examined 4,014 adult parasitic hymenopterans from different turfgrass taxa belonging to superfamilies Chalcidoidea (55% of the total wasps sampled), Platygastroidea (29%), Cynipoidea (0.05%), Ichneumonoidea (0.04%), Ceraphronoidea (0.05%), Chrysidoidea (0.01%) and Proctotrupoidea (0.004%). Eight families of Chalcidoidea, which included Mymaridae (48% of total Chalcidoidea), Trichogrammatidae (33.5%), Eulophidae (11%), Aphelinidae (0.03%), Encyrtidae (0.02%), Pteromalidae (0.02%), Eurytomidae (0.001%) and Eupelmidae (0.001%), were represented in the samples (Table 1). Mymarids, 26.5% of total wasps sampled, were largely comprised of Gonatocerus sp. and Mymar sp., and were evenly represented among turfgrass types. Gonatocerus spp. are egg parasitoids of hemipterans belonging to the suborder Auchenorrhyncha and include primary parasitoids of the glassy-winged sharpshooter, Homalodisca vitripennis (Say), in many agro-systems (Irvin and Hoddle 2005). Eulophid wasps, Aprostocetus sp. and Pnigalio sp., were less abundant in centipedegrass compared with other turfgrasses. Aprostocetus is the largest eulophid genus found in North America, parasitizing eggs of spiders, mites and nematodes (LaSalle 1994) whereas Pnigalio spp. parasitize mostly leaf miners. The role of mymarids and eulophids and impact on turfgrass pests remains unknown.
Mean (± S. E.) parasitic hymenopterans per 4.6- by 4.6-m collected from various turfgrasses (21 residential lawns) during May–July 2005 in Spalding Co., GA.
Encyrtid wasps are parasitoids of eggs and larvae of many insect and mite species and are widely used as biological control agents in many ecosystems (van Driesche et al. 2008). This family was collected from all grasses except tall fescue. The encyrtid wasps included Pseudaphycus sp., a genus containing mealybug parasitoids in nonturf systems. For example, Pseudaphycus sp. have been documented parasitizing Pseudococcus sp. mealybugs on horticultural crops (Sandanayaka et al. 2009). Reinert (1972) reported the encyrtid egg parasitoids, Eumicrosoma benefica Gahan, on southern chinch bug, B. insularis Barber, in St. Augustinegrass in Florida. He further documented an average population of 35 E. benefica associated with 90 southern chinch bugs per ft2 (0.09 m2).
Pteromalid wasps were not collected from tall fescue but were evenly collected from other grasses. Trichogrammatid wasps were more abundant in St. Augustinegrass and tall fescue than in zoysiagrass (Table 1). Oligosita sp. (Trichogrammatidae) was most numerous in tall fescue. Although there were many other unknown trichogrammatid wasp genera in our samples, host-insect association essential to specifically identify them to genus was lacking. In a similar study, Carstens et al. (2007) reported an abundance of Aphelinidae, Mymaridae, Trichogrammatidae and Braconidae on sticky traps in buffalograss. In our study, Chalcidoidea were most abundant in July with a corresponding 50.1% of total mymarids, 54.6% of total eulophids and 78.9% of trichogrammatids in July collections (Table 2). However, 96.4% of total aphelinids were recorded in May and very few or none were collected in June or July samples.
Encyrtid wasps are parasitoids of eggs and larvae of many insect and mite species and are widely used as biological control agents in many ecosystems (van Driesche et al. 2008). This family was collected from all grasses except tall fescue. The encyrtid wasps included Pseudaphycus sp., a genus containing mealybug parasitoids in nonturf systems. For example, Pseudaphycus sp. have been documented parasitizing Pseudococcus sp. mealybugs on horticultural crops (Sandanayaka et al. 2009). Reinert (1972) reported the encyrtid egg parasitoids, Eumicrosoma benefica Gahan, on southern chinch bug, B. insularis Barber, in St. Augustinegrass in Florida. He further documented an average population of 35 E. benefica associated with 90 southern chinch bugs per ft2 (0.09 m2).
Pteromalid wasps were not collected from tall fescue but were evenly collected from other grasses. Trichogrammatid wasps were more abundant in St. Augustinegrass and tall fescue than in zoysiagrass (Table 1). Oligosita sp. (Trichogrammatidae) was most numerous in tall fescue. Although there were many other unknown trichogrammatid wasp genera in our samples, host-insect association essential to specifically identify them to genus was lacking. In a similar study, Carstens et al. (2007) reported an abundance of Aphelinidae, Mymaridae, Trichogrammatidae and Braconidae on sticky traps in buffalograss. In our study, Chalcidoidea were most abundant in July with a corresponding 50.1% of total mymarids, 54.6% of total eulophids and 78.9% of trichogrammatids in July collections (Table 2). However, 96.4% of total aphelinids were recorded in May and very few or none were collected in June or July samples.
Mean (± S. E.) parasitic hymenopterans per 4.6- by 4.6-m collected using two sampling method on three dates from 21 residential lawns during May–July 2005 in Spalding Co., GA.
Platygastridae and Scelionidae were most abundant in zoysiagrass, St. Augustinegrass and bermudagrass compared with centipedegrass or tall fescue (Table 1). Platygastrid wasps (mean ± SE = 0.54 ± 0.08) collected in our turfgrass samples included Allotropa sp., which are known to be egg parasitoids of mealybug pests (Pseudococcidae) (Muesebeck 1954), and Fidiobia sp. which have not been reported on any turfgrass pest. Other studies have demonstrated the parasitic capability of the endoparasitoid, Fidiobia dominica Evans & Peña, on root weevils, Diaprepes sp., in citrus (Jacas et al. 2007) and on chrysomelid leaf beetles in other ecosystems. Scelionids comprised 22.8% of wasps among all turfgrasses sampled in the present study. In contrast, Carstens et al. (2007) reported that 66.3% of parasitoids collected in buffalograss were scelionids. A wingless scelionid, Baeus sp., was found in all turf types except tall fescue, whereas another wingless scelionid, Trimorus sp., was evenly collected from all turfgrasses. Guarisco (2001) reported Baeus sp. as a parasitoid on pirate spider, Mimetus sp., egg sacs. Carstens et al. (2007) recorded occurrence of a higher number of scelionid wasps during late- July corresponding to a second-generation of western chinch bug, Blissus occiduus Barber. In the south-eastern United States, southern chinch bug, B. insularis is a serious pest of St. Augustinegrass (Reinert 1978, Cherry 2001). More studies are required to further determine the potential of scelionid wasps for suppressing chinch bugs.
Figitids, mainly Hexacola sp., were more abundant in St. Augustinegrass than in all other turfgrasses in this study (Table 1). Eskafi and Legner (1974) observed Hexacola sp. as a parasite of the dipteran eye gnats, Hippelates sp. (Chloropidae). Emargo sp., also figitids, were evenly represented in all grass types in our study. Little is known about their role in turfgrass systems.
Both ichneumonids and braconids were captured equally in all turfgrass types except in tall fescue. Braman et al. (2004) noticed significant parasitism of first- or second-instar fall armyworm, S. frugiperda, larvae by the braconid, Aleiodes laphygmae Viereck in different turfgrasses. Parasitism was greatest in the seashore paspalum grass cultivar, ‘Sea Isle 1’, compared with bermudagrass or zoysiagrass cultivars. Occurrence of braconids, Cotesia marginiventris Cresson and Meteorus sp., was also observed on first- or second-instar fall armyworm larvae in their study. In our study, we noted greater representation of both ichneumonids and braconids in June than in July samples. Conversely, Braman et al. (2004) recorded higher events of parasitism by A. laphygmae in July than in other summer months. Other parasitic hymenopterans collected were 216 ceraphronid, 21 diapriid, and 4 cynipid wasps among all turfgrasses.
Dryinids develop within the host abdomen creating a protrusion or ‘bulged cyst’ lined by the molted skin of wasp larvae (Krombein et al. 1979). While we did not observe any dryinid wasps or dryinid-parasitized host from zoysiagrass in our samples, all the adults collected were Gonatopus sp. and were more abundant in tall fescue than any other turfgrasses sampled (Table 1). The total of 45 dryinids including both free-living adults and those within parasitized-hosts were collected during the entire season. Parasitized-hosts, cicadellids (F= 12.54; df = 4, 472; P< 0.0001) and delphacids (F = 4.16; df = 4, 473; P = 0.0025) were more abundant in tall fescue and St. Augustinegrass, respectively (Table 3). It is noteworthy that a greater proportion of the delphacids were parasitized by dryinid wasps than cicadellids in identical settings (Table 3).
Mean (± S. E.) Cicadellidae or Delphacidae parasitized by Dryinidae per 4.6- by 4.6-m during May–July 2005 in Spalding Co., GA.
Dryinid wasps parasitized leafhoppers (Cicadellidae) and planthoppers (Delphacidae) in forage-type bermudagrass (Buntin 1989). Approximately 10% parasitism occurred in that study, with peak incidence starting from May through July. We observed only 0.07% and 0.08% parasitized cicadellids or delphacids, respectively. More dryinids were captured in July than in June samples.
Vacuum sampling proved to be more efficient than sweep sampling for collecting minute Hymenoptera in our study (Table 2). However, whereas 82.2% of the total minute wasps were collected in vacuum samples, encyrtid, pteromalid, ichneumonid, braconid, diapriid and dryinid wasps were captured in similar numbers by both collecting methods.
Our results demonstrate an abundant and diverse community of parasitic wasps in residential turfgrasses in central Georgia that could be a focus of conservation efforts. More than half of the parasitoid taxa examined varied with turf type in our study, consistent with our other published data on turf taxa impact on natural enemy occurrence and abundance (Braman et al. 2003, 2004, Joseph and Braman 2009a,b). This may reflect microhabitat suitability or primary or alternate host preference for turf species. It is important to conserve parasitoids to enhance natural suppression of turfgrass pests without compromising aesthetic value. Additional research addressing impact of parasitic wasps as mediated by turf genotype may help to more effectively manage parasitoids in specific arthropod communities in the turfgrass ecosystem.
Acknowledgments
We appreciate the technical assistance provided by J. Quick, L. E. Mack and G. Braman in sample collection. The authors thank J. L. Hanula, M. D. Ulyshen and C. M. Abraham for comments on this manuscript. Matthew Buffington, identified Gonatopus sp., Emargo sp., Hexacola sp., Allotropa sp., Fidiobia sp., Baeus sp., and Trimorus sp. at the Systematic Entomology Laboratory, Agricultural Research Service, US Department of Agriculture. Similarly, Michael W. Gates helped by identifying Oligosita sp., Gonatocerus sp., Pnigalio sp., Aprostocetus sp., and Pseudaphycus sp. at the same institution. Funding for this project was provided by USDA SRIPM 34103-14551.