Print
Discovery of a non-native parasitoid, Marlattiella prima Howard (Hymenoptera, Aphelinidae) and its non-native host, Lopholeucaspis japonica Cockerell (Hemiptera, Diaspididae) in Central Texas
expand article infoKyle Gilder, Kenneth E. Masloski, James B. Woolley, Mengmeng Gu, Michael E. Merchant§, Kevin M. Heinz
‡ Texas A&M University, College Station, United States of America
§ The Texas A&M AgriLife Research & Extension Center at Dallas, Dallas, United States of America
Open Access

Abstract

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.

Keywords

biologivcal control, Marlattiella, Marlattiella prima, Lopholeucaspis 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).

Figure 1. 

Marlattiella prima Howard adult female recovered from Lopholeucaspis japonica Cockerell on Lagerstroemia indica L. trees. This specimen is in the TAMU Insect Collection (TAMUIC) as TAMU Vouchers #746. The photograph was taken by JBW with a Macropod system (https://macroscopicsolutions.com) using 20× microscope objective, a 200 mm tube lens, and a Canon EOS 5D Mark III camera.

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.

Methods

Foliage samples were collected from 40 plants of the ‘Natchez’ (Lagerstroemia indica L.) crapemyrtle cultivar and 60 plants of other crapemyrtle cultivars in Brazos County and Tarrant County, Texas. Tarrant County is 190 km north of Brazos County, and Brazos 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.

Table 1.

Numbers of Lagerstroemia indica trees with L. japonica and M. prima present.

Collection Trees with L. japonicaa Trees with M. prima present (range of M. prima recovered)b Number of M. prima present
Spring 2018 Data Not Recorded 4 (1–2) 6
Summer 2018 29 4 (1–3) 6
Fall 2018 23 1 (1) 1
Winter 2018 25 5 (1–5) 13

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). Acer spp. L. (Sapindales: Sapindaceae), Alnus spp. Miller (Fagales: Betulaceae), Ilex spp. L. (Aquifoliales: Aquifoliaceae), Liquidambar spp. L. (Saxifragales: Altingiaceae) and, Magnolia spp. L. (Magnoliales: Magnoliaceae) are among the native Texas trees (Texas A&M Department of Horticulture 2019) that L. japonica uses as a host, and sampling of these trees may yield more discoveries of L. japonica individuals in Texas.

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.

Acknowledgements

The authors would like to acknowledge our funding source, USDA grant number 2017-51181-26831/1013059. The authors would also like to acknowledge the contributions of Steven Arthurs, Silvana Caravantes, John Gilder, Patricia Gilder, Patricia Ishii, José G. Juarez, Shroq Kesbeh, Peter Krauter, Bala Sapkota, and Janaina Siqueira Da Cunha. This work is partially supported by Specialty Crop Research Initiative project ‘Systematic Strategies to Manage Crapemyrtle Bark Scale, An Emerging Exotic Pest’ [grant no. 2017-51181-26831/project accession no. 1013059] from the U.S. Department of Agriculture (USDA) National Institute of Food and Agriculture. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the USDA.

References

  • Frank SD, Klingeman III WE, White SA, Fulcher A (2013) Biology, injury, and management of maple tree pests in nurseries and urban landscapes. Journal of Integrated Pest Management 41(1): 1–14. https://doi.org/10.1603/IPM12007
  • Harsur MM, Joshi S, Pal RK (2018) Pomegranate: a new Host for the Invasive Scale Insect Lopholeucaspis japonica (Cockerell, 1897) (Hemiptera: Diaspididae) from Gujarat, India. Oriental Insects. https://doi.org/10.1080/00305316.2018.1451783
  • Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehen-Schnutz K, Gilioli G, Grégore J, Jaques Miret JA, Navarro MN, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Kertész V, MacLeod A (2018) Pest categorization of Lopholeucaspis japonica. European Food Safety Authority Journal 16(7): e05353. https://doi.org/10.2903/j.efsa.2018.5353
  • Kim J-W, Heraty J (2012) A phylogenetic analysis of the genera of Aphelininae (Hymenoptera: Aphelinidae), with a generic key and descriptions of new taxa. Systematic Entomology 37: 497–549. https://doi.org/10.1111/j.1365-3113.2012.00625.x
  • Knox G, Klingeman WE, Paret M, Fulcher A (2012) Management of pests, plant diseases, and abiotic disorders of Magnolia species in the Southeastern United States: a review. Journal of Environmental Horticulture 30(4): 223–234.
  • Krombein KV, Hard Jr PD, Smith DR, Burks BD (1979) Catalog of Hymenoptera in America North of Mexico (Vol. 1). Smithsonian Institution Press, Washington, 1198 pp.
  • Miller DR, Miller GL, Hodges GS, Davidson JA (2005) Introduced scale insects (Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. Proceedings of the Entomological Society of Washington 107(1): 123–158.
  • Rehmat T, Anis SB, Khan MT, Fatma J, Begum S (2011) Aphelinid parasitoids (Hymenoptera: Chalcidoidea) of armoured scale insects (Homoptera: Diaspididae) from India. Biology and Medicine 3(2): 270–281.
  • Rosen D, DeBach P (1970) Notes on the genus Marlattiella Howard (Hymenoptera: Aphelinidae). Mushi 43(3): 39–43.
  • Viggiani G (1985) Notes on a few Aphelinidae, with description of five new species of Encarsia Foerster (Hymenoptera, Chalcidoidea). Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri 42: 81–94.