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An Updated List of Parasitoid Hymenoptera Reared from the Bemisia tabaci Species Complex (Hemiptera: Aleyrodidae)

Abstract An updated list to the world fauna of parasitoid Hymenoptera reared from members in the Bemisia tabaci species complex (Hemiptera: Aleyrodidae) is provided. In total, 112 parasitoid species in 5 families and 7 genera are tabulated along with their global distributions. Pertinent references are given to aid in the accurate identification of these minute insects. We also reviewed published host-genera associations and consider some dubious, possibly due to contamination of rearing vessels with non-target insects or to misidentification of the host whitefly or parasitoid species.

The whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), is considered to represent a cryptic species complex of global economic importance (De Barro et al. 2011;. Two putative species are internationally distributed, Middle East-Asia Minor 1 (MEAM1; formerly biotype B or Bemisia argentifolii Bellows & Perring) and Mediterranean (MED; formerly biotype Q, and a genetic match to the original specimens collected by P. Gennadius) (Tay et al. 2012). Both have become notorious for their roles as the vectors of plant viruses to economically important crops (Lapidot & Polston 2010;Polston et al. 2014) and for their ability to develop resistance to a number of insecticides (Horowitz et al. 2005;Castle et al. 2010).
Since the initial invasion and spread of MEAM1 throughout the United States there has been a strong focus on the use of biological control agents to combat Bemisia infestations both in open-field and protected environments (Nguyen & Bennett 1995;Gould et al. 2008). The natural enemies of whiteflies include predators, parasitoids, and fungi. Arguably, the most important of these are the parasitoid Hymenoptera due to the relative ease of culture in the laboratory and the narrow host range of many species (Goolsby et al. 2005;De Barro & Coombs 2009;Pickett et al. 2013). The purpose of this paper is to provide a list of the parasitoid wasps reported to attack members of the B. tabaci species complex (Table 1).
All parasitoids known to attack B. tabaci whiteflies are hymenopteran wasps distributed between 5 families: Aphelinidae, Az-otidae, Encyrtidae, Signiphoridae (Chalcidoidea), and Platygastridae (Platygastroidea). In addition to named species, there exist numerous published records of undescribed or otherwise unidentified species in particular genera parasitizing a member of the B. tabaci species complex. These are excluded from the list herein because they potentially represent nominal species already listed, with exception to the genus Metaphycus Mercet (Encyrtidae), where accurate rearing records exist but no specific entities have been formally characterized (Evans 1993). There also are certain genera with host records that include a B. tabaci species complex member that is unlikely given known hostassociations. We discuss these taxa and our rationale for their exclusion in detail below.
The following table compiles information presented in previously published parasitoid lists while adding recent information gleaned from the literature. The number of parasitoid species reported from the B. tabaci species complex has increased significantly since 18 parasitoid species were first tabulated by Greathead & Bennett (1981). Gerling (1986) included 19 species in his review, omitting several from Greathead & Bennett (1981), while including new taxa, many of genus rank. Gerling et al. (2001) increased that number to 56, and Arnó et al. (2010) added an additional 20 species (all Encarsia and Eretmocerus) not included, reported, or described since Gerling et al. (2001). The current work continues on this theme bringing the total to 112 species with the expectation that this number will continue to grow as new species are discovered and the host ranges of named species are expanded to include members of this cryptic species complex.

Distribution of Bemisia tabaci Parasitoids
Parasitoid distribution records are numbered by geographic region following Evans (2007) and are reproduced below for ease of reference. The reader is referred to the same publication, freely available online, for in-depth information pertaining to the species listed including species synonyms, collection localities, host records, and citations. Additional information can be retrieved from John Noyes' Universal Chalcidoidea Database (http://www.nhm.ac.uk/chalcidoids) (Noyes 2014

Parasitoids of the Bemisia tabaci Species Complex
Ablerus Howard (Chalcidoidea: Azotidae) Species of Ablerus (=Azotus Howard) are most commonly recorded as primary, or hyperparasitoids, of immature Sternorrhyncha (Hemiptera) although certain species are known to attack lepidopteran eggs (Darling & Johnson 1984) and the pupae of chamaemyiid Diptera (Blanchard 1936). Material bred from whiteflies is typically assumed to be hyperparasitic on aphelinid primary parasitoids developing in the same host (Viggiani 1982;Evans 2007). Recently, Ablerus macrochaeta Silvestri was reported from B. tabaci in Guangxi and Yunnan Provinces in the People's Republic of China following a 10 yr natural enemy census (Li et al. 2011). Additional whitefly host records for A. macrochaeta include Aleurocanthus inceratus Silvestri, and the citrus blackfly, Aleurocanthus woglumi Ashby. The only other instance of an Ablerus species attacking a whitefly in the genus Bemisia is Ablerus inquirenda Silvestri parasitizing Bemisia (as Lipaleyrodes) euphorbiae (David and Subramaniam) (Evans 2007).

Cales Howard (Chalcidoidea: Aphelinidae)
Cales is a relatively poorly known genus whose members, where host relationships are known, are primary parasitoids of aleyrodine whiteflies. Cales are morphologically conserved and character poor making their identification difficult without the use of molecular tools (Mottern 2012). Abd-Rabou (1997, 2002 reported a Cales sp. from B. tabaci in Beni-Suef, Egypt, citing rare incidence. At least one species, Cales noacki Howard, is globally distributed having been implemented in successful biological control programs for control of woolly whitefly, Aleurothrixus floccosus (Maskell), a severe pest of Citrus in many countries (Meyerdirk et al. 1980;Miklasiewicz & Walker 1990;Rose & DeBach 1994). This same species was reared from the B. tabaci complex in Tanzania on cassava (Manihot esculenta Crantz) (Guastella et al. 2014). It is important to note, however, that recent morpho-molecular analyses have identified C. noacki as a cryptic complex composed of at least 9 other species, some of which are indistinguishable morphologically (Mottern & Heraty 2014).

Encarsia Förster (Chalcidoidea: Aphelinidae)
Encarsia is the most speciose genus of Aphelinidae with more than 450 described species which mainly parasitize either whiteflies (Aleyrodidae) or armored scale insects (Diaspididae). The number of species recorded from the B. tabaci species complex has greatly increased over recent years from the 35 listed in Gerling et al. (2001), to 55 in Arnó et al. (2010) to 81 here. Minus a few exceptional cases, female Encarsia are primary endoparasitoids whereas males develop as ectophagous hyperparasitoids on conspecific or heterospecific individuals including those of other genera (Walter 1983;Hunter & Woolley 2001). The hostassociations of females appear to be obligate insomuch as they are restricted to a particular host family (e.g., Aleyrodidae; Diaspididae; Hormaphididae) (Polaszek et al. 2009). Conversely, although male Encarsia are usually reared from the same host(s) as the females, they have also been obtained from alternative hosts, including soft scales (Coccidae) (Myartseva & Evans 2007 Identification aids to Encarsia species are available for the following localities: Australia (Schmidt & Polaszek 2007), China (Huang & Polaszek 1998), Egypt (Polaszek et al. 1999), Hispaniola (Evans & Serra 2002), Italy (Viggiani 1987), India (Hayat 2011), Mexico (Myartseva & Evans 2007), North America (Schauff et al. 1996), and Taiwan (Shih et al. 2008). Polaszek et al. (1992) and Evans & Polaszek (1997) treated the species parasitizing the B. tabaci species complex. Heraty et al. (2008) recently discussed the systematics and biology of Encarsia with an emphasis on those attacking Bemisia species.

Eretmocerus Haldeman (Chalcidoidea: Aphelinidae)
The genus Eretmocerus contains 78 nominal species all of which are solitary, obligate, primary ecto-endoparasitoids of the whitefly subfamily Aleyrodinae. Myriad undescribed species exist including several that have been reared from Bemisia (Zolnerowich & Rose 2008). Twentythree of the 78 described species have reportedly been reared from the B. tabaci species complex. In our list, we exclude 3 species that continue to be, or have been, commonly recorded as parasitizing B. tabaci, namely Eretmocerus californicus Howard, Eretmocerus corni Haldeman, and Eretmocerus haldemani Howard. We follow the convention of Zol-nerowich & Rose (2008) that these taxa, or their host whitefly, are being misidentified (Rose et al. 1996;Rose & Zolnerowich 1997a).
Recent efforts have been made to utilize Eretmocerus in biological control programs against B. tabaci MEAM1 at the international level. Five exotic species were released in the United States for control of MEAM1 in Florida, Texas, Arizona, and California (Nguyen & Bennett 1995;Gould et al. 2008). Following the success of one of these species, Eretmocerus hayati Zolnerowich & Rose, importation for evaluation and/or releases have been made in Australia (De Barro & Coombs 2009), Egypt (Abd-Rabou 2004, the People's Republic of China (Yang & Wan 2011), and Tanzania (Guastella et al. 2014). Accurate identification of Eretmocerus depends, in large part, on the examination of properly curated material (Rose & Zolnerowich 1997a). Keys to species have been produced for the following world regions: Australia (De Barro et al. 2000), China (Wu et al. 2009), Egypt (Abd-Rabou & Evans 2002), India (Hayat 1972(Hayat , 1998, Iran (Abd-Rabou et al. 2005), Italy (Viggiani & Battaglia 1983), Mexico (Myartseva 2006a), and the United States (Rose & Zolnerowich 1997a,b;Zolnerowich & Rose 1998).

Metaphycus Mercet (Chalcidoidea: Encyrtidae)
Metaphycus are primary endoparasitoids of scale insects in the Coccoidea, although a few New World species are known to parasitize whiteflies (Myartseva 2006b) and jumping plant lice (Hemiptera: Triozidae) (Guerrieri & Noyes 2000). An as yet undescribed Metaphycus sp. was reared from B. tabaci collected in Venezuela by F.D. Bennett, providing the first record of the genus attacking an aleyrodid (Evans 1993). A recent survey of whitefly natural enemies conducted in Columbia also yielded a Metaphycus sp. (Bellotti et al. 2005). In the continental United States, there exists at least a single species capable of parasitizing B. tabaci. Recently, specimens were reared from B. tabaci (presumably MEAM1) as part of a survey of the parasitoid Hymenoptera associated with the B. tabaci species complex in southwest Florida (Z. Lahey, unpublished data). In all instances, the adults emerged through a hole chewed in the side of the whitefly and not through the dorsum, which is the typical escape route of whitefly parasitoids. This unusual emergence behavior may be explained, in part, by the subsequent rearing of the same species from a mealybug (Hemiptera: Pseudococcidae) found inhabiting the same host plant, Pluchea baccharis (Miller) Pruski (Asterales: Asteraceae). This bi-parental species probably utilizes B. tabaci facultatively and is so infrequently collected from the whitefly that it is not of economic importance.
The species of Metaphycus known to attack whiteflies are all from the New World with those that are described known solely from the Neotropical realm. A key to those species is available in Myartseva (2006b), but many remain undescribed (Guerrieri & Noyes 2000).

Signiphora Ashmead (Chalcidoidea: Signiphoridae)
Signiphora is a relatively small genus that contains primary and hyperparasitoids, most of which are distributed throughout the Neo-tropics (Woolley 1988). Signiphora aleyrodis Ashmead has been reared in small numbers from B. tabaci in numerous surveys throughout the Neotropics (Schuster et al. 1998;Viscarret et al. 2000;de Oliveira et al. 2003) and represents the only nominal signiphorid associated with the species complex. This species is an obligate hyperparasitoid of Aphelinidae and Platygastridae (Woolley 1988). Additional reports of unidentified Signiphora species reared from the B. tabaci complex exist from Cuba (Castineiras 1995), Columbia (Bellotti et al. 2005), Martinique (Ryckewaert & Alauzet 2002), and Argentina (Viscarret et al. 2000).
A key to the species and species groups of Signiphora is provided in Girault (1913) and Woolley (1988), respectively.

Amitus Haldeman (Platygastroidea: Platygastridae)
Amitus is 1 of 3 genera of whitefly parasitoids in the Platygastridae, all of which are primary endoparasitoids of whiteflies. Of the 19 species that comprise the genus, 4 (bennetti, fuscipennis, hesperidum, and longicornis) are recorded as parasitoids of B. tabaci. Amitus bennetti Viggiani & Evans was introduced into Florida from Puerto Rico for control of MEAM1 in the early 1990's (Nguyen & Bennett 1995). Although recoveries were made several weeks after initial field releases, it is unknown if this species established. Surveys conducted in southwest Florida in the mid 1990s, and from 2012-2013 did not recover this species, or any other species of Amitus, from B. tabaci (Stansly et al. 1997;Z. Lahey, unpublished data). Amitus fuscipennis MacGown & Nebeker is a well-known parasitoid of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and appears capable of utilizing B. tabaci in the laboratory (reference in Gerling et al. 2001); to our knowledge A. fuscipennis has never been reared from B. tabaci in the field. Both A. hesperidum Silvestri and A. longicornis (Förster) parasitize citrus pests in the genus Aleurocanthus Quaintance. Additional Amitus have been reared from B. tabaci in Honduras (Vélez 1993) and Nicaragua (Nunes et al. 2006).
Identification of Amitus is difficult due to a lack of information regarding the genus. Viggiani & Mazzone (1982) provided a key to the species of Italy. MacGown & Nebeker (1978) reviewed the species of the Western Hemisphere, and Polaszek (1997) discussed the European species. Some of the New World species were addressed by Viggiani & Evans (1992).

Doubtful Reports
One species from each of the following 3 chalcidoid genera are recorded as parasites of the B. tabaci species complex: Adelencyrtus Ashmead (Encyrtidae), Neochrysocharis Kurdjumov (Eulophidae), and Pteroptrix Westwood (Aphelinidae). Adelencyrtus are parasitoids of Coccoidea (mostly Diaspididae), with 1 doubtful record of A. moderatus (Howard) from B. tabaci (Greathead & Bennett 1981). To our knowledge, A. moderatus, as well as any other species of Adelencyrtus, has never reliably been reared from an aleyrodid. Most likely the whitefly collection that produced these specimens was contaminated with diaspine scales resulting in this host association.
A similar situation arises in regards to Pteroptrix, also parasitoids of Diaspididae. Like the genus Encarsia, Pteroptrix exhibit heteronomous life histories with females acting as primary parasitoids and males developing as hyperparasitoids on the same or different species (Hunter & Woolley 2001). If females are capable of utilizing parasitized whiteflies as hosts for males, rearings of male but not female Pteroptrix from aleyrodids could be possible. Both Pruthi & Samuel (1942) and Samuel (1950) included P. bemisiae Mani as a B. tabaci parasitoid in India. Hayat (1986) considered this species a nomen nudum, and for this reason alone it cannot be included as a valid parasitoid of the B. tabaci complex. In addition, no other species of Pteroptrix appears to be associated with whiteflies, making the relationship between P. bemisiae and B. tabaci unlikely.
The eulophid genus Neochrysocharis was added to the list of whitefly parasitoids following reported rearings from the 3 whitefly species, Aleyrodes proletella L., Bemisia tabaci (Gennadius), and Tertalicia erianthi Danzig, in central Asia (Myartseva 1993;Myartseva & Yasnosh 1994). Typical host-associations for Neochrysocharis species include leaf-mining Diptera and Lepidoptera, although other taxa have also been cited (Noyes 2014). Arguably the most well-known and polyphagous species is N. formosus (= formosa Westwood), which has been bred from over 100 different host species in 5 orders (Luna et al. 2011). Although we do not completely exclude the possibility of N. formosus as a valid parasitoid of the B. tabaci species complex, or of whiteflies in general, we evince caution in doing so for the following reasons; (i) no other species of Neochrysocharis has been associated with the Aleyrodidae; (ii) primary whitefly parasitism in the family Eulophidae appears to be restricted to the tribe Euderomphalini; (iii) N. formosus and certain members of the B. tabaci complex have a cosmopolitan distribution and can be found within the same agricultural environment on the same host plant(s). Unless N. formosus displays an affinity for parasitizing a species of the B. tabaci complex endemic to the collection locality, one would expect subsequent collecting efforts to have produced N. formosus specimens from B. tabaci on at least one other occasion somewhere else in the world.

Conclusions
The B. tabaci species complex remains a serious economic problem worldwide despite the considerable attention gained over the past 30 yr. Fortunately, the number of potential biocontrol agents used for control of these pest whiteflies continues to grow as new species are discovered and the host range of known species is expanded to include members of this cryptic species complex. In this regard, the genus Eretmocerus leads the way as the most important group of parasitic wasps used against B. tabaci whiteflies with Er. hayati having been introduced onto 3 continents outside its native range. It is our hope that the current work will serve as an important reference for biocontrol workers in regards to general information about the genera that parasitize B. tabaci whiteflies, as a portal to the references that allow for their accurate identification, and as a starting point for the construction of a comprehensive key to the species that help control this serious pest complex of world agriculture.