A key to the flat grass scale genus Nipponaclerda (Hemiptera, Coccomorpha, Aclerdidae)

Abstract The flat grass scale genus Nipponaclerda comprises four species, native to Central and East Asia. Nipponaclerdabiwakoensis has been introduced to the United States and is considered a serious pest of Phragmitesaustralis, the common reed. Heavy infestations of N.biwakoensis in coastal marshes of Louisiana have coincided with extensive die-off of reeds. In this article, dichotomous identification keys to the genera of Aclerdidae and to the species of Nipponaclerda are provided, allowing for accurate identification of species found in the native and invasive range.


Introduction
The genus of flat grass scale insects, Nipponaclerda McConnell (Hemiptera, Coccomorpha, Aclerdidae), comprises four species native to Central and East Asia, one of which has been introduced to the United States.This small group is receiving attention due to the recent discovery of Nipponaclerda biwakoensis (Kuwana) (the roseau cane scale) in Louisiana, U.S.A. (Knight et al. 2018).The detection of invasive populations of N. biwakoensis in Louisiana coincided with the discovery of extensive die-off of Phragmites australis (Cav.) Trin. Ex Steud. (i.e., common reed, roseau cane).In 2016, surveyors found large stands of dead or dying P. australis in Plaquemines Parish, Louisiana (Knight et al. 2018), part of the Mississippi River Delta (MRD).This sparked concern due to the reeds' importance to marsh ecosystems and coastal infrastructure.Losses of Phragmites in the MRD could have substantial, negative economic repercussions.Roseau cane is the dominant emergent plant in the MRD; it builds, maintains, and protects marsh soils and provides habitat for diverse wildlife.Dense stands of roseau cane help reduce wave action, which shields coastal regions from damaging storm surges and hurricanes.The marshes also shelter a network of shipping channels as well as oil and gas infrastructure in this region.
Presently, N. biwakoensis is the only member of this genus to be considered a pest.Heavy infestations in Louisiana reached over 2,000 individuals per stem in 2016-2017 (Knight et al. 2018).In China it is considered a pest of P. australis, which is cultivated for the paper industry (Brix et al. 2014).Natural enemies help keep populations at low abundance in the native range, and in Japan and China N. biwakoensis served as a model for studies about parasitism by hymenopterans and predation from birds (Kaneko 1995;2004;2005;Xiong et al. 2010).
Aclerdids feed primarily on grasses (Poaceae), which include some of the most important commodities such as maize, rice, wheat, and sugarcane.But damaging infestations of aclerdids are uncommon on commodities (McConnell 1954), which explains why aclerdids have received minimal attention in the taxonomic literature, where efforts skew toward larger groups with more significant agricultural impact.Thus, Aclerdidae is an especially difficult group to identify to species.The only key ever published to differentiate between species of Nipponaclerda was by Borchsenius (1960), which can be used to separate N. biwakoensis from N. turanica (Archangelskaya) (reproduced in Wang 1994).Considering the potential economic impact of N. biwakoensis, a history of introduction to the United States, and the possibility of discovering additional species, it is important to have a tool that allows for accurate identification of species in this genus.

Materials and methods
Specimens of N. biwakoensis collected from Louisiana and Texas were slide-mounted following the protocol of the Systematic Entomology Laboratory (USDA, ARS) at Beltsville, Maryland (http://www.ars.usda.gov/Main/docs.htm?docid=9832).DNA extractions were performed on some specimens prior to slide-mounting (see Knight et al. 2018); others were prepared without having an extraction performed.Specimens are deposited in the United States National Museum of Natural History's Collection of Coccomorpha, housed in Beltsville, Maryland.Observations were made using a Zeiss Axio Imager.M2 (Carl Zeiss Inc., Thornwood, NY, U.S.A.).Diagnostic information for species of Nipponaclerda was drawn from published descriptions and illustrations (Borchsenius 1960;Kuwana 1907;McConnell 1954;Wang and Zhang 1994;Zhang 1998).(Hodgson and Millar 2002), with Aclerda Signoret and Lecanaclerda Hodgson & Millar.Members of this genus are similar to species of Aclerda but can be distinguished in the adult female stage by the poor development of anal ring setae, which are few in number, shorter than the anal plate, and never extend beyond the body apex (Borchsenius 1960).In adult females of Aclerda, these setae are numerous, long, and usually protrude beyond the posterior body margin; however, these setae fail to extend beyond the margin in A. pasquieri Balachowsky, A. sinaloaensis McConnell, and A. subterranea Signoret.Additionally, dorsal conical pores (referred to as invaginated setae in McConnell 1954) can be found in species of Aclerda but are absent from Nipponaclerda.There are no discernable differences between the immature instars of these two genera but adult males of Nipponaclerda can be differentiated by the encircling marginal setae, absence of dorsal invaginated conical pores, and reduction in the number of anal ring setae (McConnell 1954).The adult male stage has only been described for N. biwakoensis.

Species list
Nipponaclerda biwakoensis (Kuwana, 1907: 187) Nipponaclerda leptodermis Wang & Zhang, 1994: 94 Nipponaclerda triumpha Zhang, 1998: 7 Nipponaclerda turanica (Borchsenius, 1950: 156) Nipponaclerda biwakoensis (Kuwana, 1907 Notes.Adult females of N. biwakoensis are similar in appearance to N. turanica but the two can be easily distinguished by the traits mentioned above, and in addition by the pattern of sclerotization and by the types of setae located on the anal plate and posterior margin.The posterior end is heavily sclerotized in N. turanica, whereas in N. biwakoensis, moderate sclerotization is more evenly distributed along the marginal rim, becoming more heavily sclerotized in mature females.N. biwakoensis possesses some tuberculate setae on the anal plate and bears only tuberculate or spine-like setae on the posterior body margin.In contrast, only flagellate setae are present on the anal plates of N. turanica and several flagellate setae fall on the posterior body margin.N. biwakoensis was well-illustrated by McConnell (1954); additional illustrations were published by Kuwana (1907;1932) and Wang (1994).
It is difficult at present to determine the origin and timing of invasion to the United States.Specimens of N. biwakoensis were encountered in quarantine interceptions originating from Japan three times in California andonce in Hawaii, between 1959 and1961.But populations have only been collected from the U.S. since 2016 (Knight et al. 2018), suggesting their establishment is a recent event.Infestations have been found in Louisiana and eastern Texas on Phragmites australis, which appears to be the primary host for this species.N. biwakoensis was also reported on species of Agropyron and Juncus (Wang 1994), but these host records should be confirmed through further sampling.