New species of Eretmocerus Haldeman (Hymenoptera: Aphelinidae) parasitizing Crenidorsum turpiniae (Takahashi) and Aleurothrixus floccosus (Maskell) (Hemiptera: Aleyrodidae) from Taiwan

Abstract A key to females of 11 Eretmocerus species occurring in Taiwan is provided. Two new species, E. tongxiaoensis Shih & Polaszek, sp. nov. and E. lannae Shih & Polaszek, sp. nov. found infesting Crenidorsum turpiniae (Takahashi) and Aleurothrixus floccosus (Maskell) respectively, are described. Five more Eretmocerus species are recorded here as new to Taiwan: E. bisetae Hayat, E. flavus Krishnan & David, E. queenslandensis Naumann & Schmidt, E. rui Zolnerowich & Rose and E. trialeurodis Hayat. New host records for four of these Eretmocerus species from five whitefly species are presented. The whitefly Aleurothrixus floccosus (Maskell) is recorded for the first time from Taiwan.


Introduction
Species of Eretmocerus Haldeman develop as primary ecto-endoparasitoids of whiteflies (Rose and Rosen 1992). The genus Eretmocerus comprises 81 species worldwide, of which three species were previously recorded from Taiwan (Noyes 2015). This paper brings the total number from Taiwan to 11.
Eretmocerus species have been relatively successful as classical biological control agents of several whitefly species, and have been utilized in effective biological control programmes, especially for the global pest complex Bemisia tabaci (Rose et al. 1996;Rose and Zolnerowich 1997). At least two species of Eretmocerus (E. eremicus Rose & Zolnerowich and E. mundus Mercet) are available commercially (Liu 2007). Eretmocerus species appear to be diverse in Taiwan, indicating their potential for commercial production for pest control. In 2004-2014 we recorded 10 Eretmocerus species from seven species of whiteflies (A. floccosus (Maskell), B. tabaci (Gennadius), Bemisia emiliae (Chen & Ko), Bemisia porteri Corbett, Trialeurodes vaporariorum (Westwood), Aleurotrachelus turpiniae (Takahashi), Dialeurodes citri (Ashmead)). Sometimes they outnumber, and are more effective than, Encarsia species, e.g. E. furuhashii on B. emiliae. Hayat (1998) provided a key to females, and descriptions of Indian species of Eretmocerus, including species from the Oriental region. However, previous taxonomic studies on Eretmocerus species from Taiwan have been restricted to a few references reporting the use of E. orientalis in biological control of B. tabaci and T. vaporariorum (Chou et al. 1999;Lin et al. 2002;Shih et al. 2008). Reviews of the Eretmocerus species from China included references to the occurrence of species in Taiwan (Huang and Huang 2004;Wu et al. 2009). Eretmocerus species from Taiwan are to some extent similar to those from Fujian province (China), of which only E. furuhashii, E. mundus and E. orientalis were known previously from Taiwan (Huang 1994;Huang and Huang 2004;Wu et al. 2009;Noyes 2015 Hayat. Goolsby et al. (2000) recorded E. melanoscutus Zolnerowich & Rose from Taiwan, but voucher specimens for this record were not examined during the present study. The inclusion of this species is therefore based on examination of paratype material from Thailand, and the original description.

New record of a whitefly pest
Aleurothrixus floccosus (Maskell) invaded Taiwan in 2013 or earlier, and is currently causing serious damage to the golden dewdrop: Duranta repens L. and guava: Psidium gujava L. Duranta repens is a popular ornamental plant in Taipei, and there was no record of whiteflies from this plant before the invasion of the woolly whitefly. Occasionally, large populations cause leaf-wilting of D. repens in North Taiwan. A. floccosus is now well-established in Central and Northern urban areas. However, chemical control for A. floccosus is not advisable for public and environmental health reasons, and biological control appears to present a potential method to control it (DeBach and Rose 1976;Meyerdirk et al. 1980;Onillon 1988).

Survey, collection and identification of parasitoid hosts
A series of surveys was undertaken from 2004 to 2014 for the collection of parasitoid host whiteflies, scale insects and aphids in Taiwan. Whiteflies were identified by C.C. Ko. Our field experience indicated that populations of Eretmocerus species were higher in urban areas, outskirts and farm land, probably due to fewer host competitors, particularly B. tabaci, and natural enemies.

Rearing of parasitoids
Rearing parasitoids from their hosts provides most of the information on their biology, behaviour and ecology. In order to get the precise host information, the whitefly infested leaves were cut into small pieces and placed separately in small transparent glass tubes. On confirmation of the host from which parasitoids emerged, several infested pupal cases were placed in larger jars and covered with cotton or zip-lock covers. Zip-lock bags were found to be an ideal container, as the emerged parasitoids entered the edges of the bags, making it easier to find them. Parasitoids were transferred to 95% alcohol using a fine brush without damaging the specimens. Using this method, the zip-lock bags need replacing and should not be reused.

Preservation of parasitoids
We recommend that adult Eretmocerus specimens are preserved in 95% alcohol in a refrigerator set below 4°C. Dry preservation or similar methods may cause distortion of characters. Although many authors have suggested 70% alcohol is the best concentration (Noyes 1982), we prefer to use the higher concentration, which in our experience minimizes errors during mounting; specimens preserved in this way are also suitable for molecular sequencing. Identification of Eretmocerus species is frequently problematic irrespective of mounting method (card or slide) due to their very weak sclerotization compared with most other aphelinid genera.

Terminology
Morphological terminology and the format for species descriptions follow Rose and Zolnerowich (1997) and Zolnerowich and Rose (1998). We have made some minor modifications, e.g. focusing on characters of the head, and the fore and hind legs. Basic morphological characters for females are: Antenna: length of clava (C), especially relative to its width; length and shape of first funicle segment (F1); length and shape of second funicle segment (F2); length of pedicel (P); length of radicle (R); length of scape (S). Wing: length of fore wing (L), length of marginal vein (M), length of submarginal vein (SM), length of stigmal vein (ST), greatest width of disc (W), especially relative to the longest posterior alar fringe. Mesosoma: length of mid lobe (ML); greatest width of mid lobe (WM); length of scutellum (SC); greatest width of scutellum (WS). Gaster (metasoma minus petiole): length of gaster (G), arrangement of paired setae on tergites 2-6. Leg: length of mid tibia (MT).
Line drawings were made using an Olympus BX51 compound microscope and scanning electron microscope (SEM) images taken using microscope (ZEOL S-800; Tokyo, Japan) located in the Department of Entomology, National Taiwan University (NTU), Taipei, Taiwan.

Depositories
The holotypes and paratypes of the new species are deposited in the Department of Entomology, NTU. Some paratypes are additionally deposited at the Natural History Museum, London (BMNH) (E. queenslandensis appears twice in the key deliberately).

Diagnosis
Females of Eretmocerus lannae sp. nov. can be identified by having 6 setae on the mesoscutum; a single seta on each mesoscutal side lobe; a short, pale yellow, cylindrical antennal clava, 4.7-5× as long as wide ( Figure 1C); and prominent frenal arms (circled in Figure 3).
Colour. Head yellow. Mesosoma pale yellow. Gaster yellow. Antenna pale yellow. Wings hyaline. Legs pale yellow except basal margin of mid and hind femur.

Remarks
The female of Eretmocerus lannae sp. nov. is unusual in having a single seta on the mesoscutal side lobe, a character observed for the first time in the genus Eretmocerus. Generally, Eretmocerus species have 2-3 setae on the side lobe. The new species is close to E. trialeurodis Hayat, but differs from it in the length of ovipositor, which is 0.86× clava length and subequal in length to the mid tibia, and in having the mid tibial spur 0.52× the basitarsus, and with fewer setae on the vertex. Eretmocerus lannae sp. nov. is a potential biocontrol agent of A. floccosus; the parasitoid population was found to be abundant. Although A. floccosus was infesting heavily both the golden dewdrop (D. repens) and guava (P. guajava), only the population on guava was parasitized by E. lannae. The reason for this selective host preference could be plant secondary metabolites, or possibly that the population of A. floccosus on golden dewdrop secretes more wax than the guava population, creating unfavourable conditions for parasitization.

Etymology
The species name lannae is derived from 'lanna' a Latin word for 'lobe', reflecting the prominent frenal arms.
Eretmocerus tongxiaoensis Shih & Polaszek, sp. nov. (Figures 4, 5) Diagnosis Females of E. tongxiaoensis sp. nov. can be identified by having 6 setae on the mid lobe of the mesoscutum; an elongate, brown, cylindrical antennal clava, 7.1-7.88× as long as wide ( Figure 4C); a long ovipositor which is approximately the same length as the clava; and a narrow fore wing, about 2.53× as long as wide ( Figure 5D). Among the known Eretmocerus species from Taiwan, only E. orientalis Gerling has brown antennae, but has 4 setae on the mid lobe of the mesoscutum. All other Eretmocerus species in Taiwan have pale yellow or yellow antennae. E. tongxiaoensis shares having 3 paired setae laterally on T6 with E. queenslandensis, from which it differs by a shorter maximum fore wing fringe (0.25x wing disc; >0.3 in E. queenslandensis).
Antenna ( Figure 4C). Radicle 3.6× as long as wide; scape 3.5× as long as wide, 2.70× as long as radicle, 1.84× of pedicel length, 0.54× of clava length; pedicel 2.88× as long as wide, 1.50× as long as radicle, 0.54× of scape length. Funicle I triangular-trapezoid, dorsal length 0.4× ventral length. Funicle II wider than long. Clava cylindrical, narrowed at apex, 5.0× as long as greatest width, 1.83× of scape length, 3.69× of pedicel length.  Scape with one large sensillum close to the end. Clava with one large longitudinal sensillum and one thick sensillum close to the clava apex. Clava with 7 articulated spines.
Mesosoma ( Figure 5A). Mid lobe of mesoscutum with 6 setae, anterior part with cellular reticulate sculpture, remainder with faint elongate reticulations. Each side lobe with 3 setae, anterior margins with elongate cellular reticulations; axilla with 1 seta, strongly reticulate. Scutellum with 4 setae, anterior pair shorter, 2 placoid sensilla laterally, closer to the posterior pair of setae, and sides with faint, elongate reticulations. Frenal arms short and not exceeding metanotum. Metanotum slightly narrower centrally than propodeum. Propodeum with strong transverse reticulations, central lobe broad and smooth, reaching half the length of gastral tergite I.

Remarks
Eretmocerus tongxiaoensis resembles E. rui Zolnerowich & Rose (2004), but differs from it in having antennae and T7 brown (antennae and T7 are yellow in E. rui).

Etymology
The species is named after the type locality Tongxiao. Residents of this area kindly helped during collection.