Discovery of a non-native parasitoid and its non-native host in Central Texas 213 Discovery of a non-native parasitoid, Marlattiella prima Howard (Hymenoptera, Aphelinidae) and its non-native host, Lopholeucaspis japonica Cockerell (Hemiptera, Diaspididae) in Central Texas

Sampling of crapemyrtle trees (Lagerstroemia L.) in central Texas yielded the discovery of an invasive scale pest, Lopholeucaspis japonica Cockerell, and its parasitoid natural enemy, Marlattiella prima Howard. These discoveries expand the known range of both the scale insect and the parasitoid wasp in the United States. Marlattiella prima was not recovered in the absence of L. japonica. Of the two counties sampled, Brazos County yielded 26 M. prima individuals and Tarrant County yielded neither M. prima nor L. japonica.


introduction
Members of the genus Marlattiella Howard (Hymenoptera: Aphelinidae) are known to parasitize only armored scale insects (Hemiptera: Diaspididae). Two species have been described worldwide (Viggiani 1985;Rehmat et al. 2011): M. prima Howard and M. maculata Hayat. Marlattiella prima is a parasitoid of Lopholeucaspis japonica Cockerell (Japanese maple scale) in China and Japan (Rosen and DeBach 1970) and M. maculata is a parasitoid of Aonidiella orientalis Newstead (Oriental yellow scale) in India (Rehmat et al. 2011). Viggiani (1985) identified chalcidoid wasps collected from sticky traps in Africa and uncovered a possible third species, extending the geographical range of the Marlattiella genus to the Ethiopian region.
Marlattiella prima adults closely resemble adults in the genus Aphytis Howard, and other genera in the tribe Aphytini (Kim and Heraty 2012). Marlattiella spp. individuals are distinguished from the other members of Aphytini by their antennal formula: scape, pedicel, no funicle segments or anelli, and a long, unsegmented clava ( Figure 1). Species of Eretmocerus Haldeman, a similar and closely related genus (Kim and Heraty 2012), share this antennal formula but have four-segmented tarsi while Marlattiella spp. have five-segmented tarsi. Additional recognition characteristics include a short propodeum in Marlattiella spp. lacking the marginal crenulae found in Aphytis spp. (Rosen and DeBach 1970) (Figure 1).
Lopholeucaspis japonica (Hemiptera: Diaspididae) was first reported in the United States in Connecticut in 1914 (Miller et al. 2005). Currently the reported distribution of this scale in the United States includes Connecticut, Delaware, Georgia, Kentucky, Louisiana, Maryland, New Jersey, New York, North Carolina, Pennsylvania, Rhode Island, Tennessee, Virginia, and Washington DC (Frank et al. 2013;Jeger et al 2018). It has a host range of approximately 97 plant species from 35 families (Knox et al. 2012;Harsur et al. 2018;Jeger et al. 2018). In the United States, M. prima has been reported in Maryland, only one of the fifteen states in which L. japonica has been reported (Krombein et al. 1979). This paper describes the first reported occurrences of L. japonica and M. prima in Texas. This is important because it expands the range of a pervasive pest of 97 tree species as well as the range of one of its known parasitoids. County is approximately 158 km NE of Houston, Texas. Ten 30 cm long branch tips randomly distributed along the canopy perimeter of three-meter to five-meter-tall trees were collected using a telescoping pruner with a 2.7 m reach. Branch tips were immediately placed in Sure Fresh rectangular storage containers, 10 cm × 35 cm (Greenbrier International, Inc., 1509 Sam's Circle Store No 502 Chesapeake, VA 23320-4694 United States, www.dollartree.com, SKU: 236854). Storage containers were labelled by tree. Each tree was given a unique number and GPS data was collected using a cellphone application (GPS Status & Toolbox Pro version 9.0.183 2019, EclipSim). The GPS coordinates were recorded for the purpose of using the same trees every season from spring 2018 to winter 2018.
The plastic containers containing branch samples were placed in cold storage for 24 to 120 hours at 6 °C to slow down arthropods during the sample processing period. Containers removed from cold storage were opened and branches were carefully examined with the aid of a stereo microscope (Olympus SZ-6045). Scale insects were counted and identified to the lowest taxon possible.
Branches were subsequently placed in sealed, white paper bags (Uline white grocery bags, uline.com model no. S-11541, 19.685 cm × 12.065 cm × 40.64 cm) to allow for parasitoid emergence. After three months, the bags were opened and the contents were shaken into a petri dish containing 70% ethanol. Using a stereo microscope (Olympus SZ-6045), parasitoids were then counted and identified to the lowest taxonomic level possible before being placed in labelled vials with 70% ethanol for preservation. Voucher specimens have been deposited in the TAMU Insect Collection (TAMUIC) as TAMU Vouchers #746.

results
A total of 26 M. prima individuals were recovered from 400 L. indica samples in Brazos County (Table 1). Most were recovered from samples collected during winter of 2018. All of the L. indica twigs from which Marlattiella individuals were recovered contained Lopholeucaspis japonica individuals, with the exception of those collected in the spring of 2018, for which there are no data on scale presence. Lopholeucaspis japonica were frequently recovered from the same locations and trees across all four seasons. No L. japonica or M. prima were recovered from 400 samples taken in Tarrant County.

Discussion
Our collections represent the first occurrence of both L. japonica and M. prima individuals in Texas. The range of L. japonica around Brazos County may be indicative of a population existing prior to our detection. The fact that it was recovered from the same trees at the same locations may imply that it is not rapidly spreading, though only L. indica plants were sampled and it is known that L. japonica has a wide host range (Knox et al. 2012;Harsur et al. 2018;Jeger et al. 2018)

Conclusion
Surveys from Brazos County, TX document the presence of Lopholeucaspis japonica and Marlattiella prima, which have not previously been reported for Texas. This record expands the range of both organisms. The population of L. japonica is apparently not spreading, as it remained localized on a set number of trees in Brazos County and was not found in Tarrant County. A total of 100 trees were sampled for each collection and a total of 35 trees across all collections hosted L. japonica. Values within the column are the number of trees infested with L. japonica within a collection. b Range represents the minimum and maximum of M. prima recovered from trees infested by L. japonica within a collection.