Tetralicia Harrison, 1917

Valencia, Luis & Evans, Gregory A., 2024, Review of the genus Tetralicia (Hemiptera: Aleyrodidae) and description of two new species of whiteflies found on avocado trees in Peru, Zootaxa 5403 (2), pp. 197-238 : 205-209

Tetralicia Harrison, 1917

Tetralicia Harrison, 1917: 60 . Type species, Tetralicia ericae Harrison, 1917 , by monotypy.

Aleuropleurocelus Drews & Sampson, 1956: 282 . Type species, Aleuropleurocelus laingi Drew & Sampson, 1956 , by original designation; n. syn.

Harrison (1917) erected the genus Tetralicia with Tetralicia ericae Harrison, 1917 as the type species. Until now, the genus has contained six Old World species known from the Western Palearctic, Afrotropical and Australian zoogeographic regions: Tetralicia debarroi Martin & Carver, 1999 in Martin (1999) described from Australia, Tetralicia erianthi Danzig, 1969 from Turkmenistan, Tetralicia ericae Harrison, 1917 from England, Tetralicia iberiaca Bink-Moenen, 1989 from Portugal, Tetralicia graminicola Bink-Moenen, 1983 and Tetralicia tuberculata Bink-Moenen, 1983 both from Chad; Tetralicia sawyeri n. sp. found on avocado in Peru is described herein.

Drews & Sampson (1956) erected Aleuropleurocelus , a New World genus, in which they placed A. laingi Drews & Sampson, 1956 (the type species) and two other species, A. ceanothi ( Sampson, 1945) and A. sierrae ( Sampson, 1945) . Later, Drews & Sampson (1958) described four additional new species, A. acaudatus Drews & Sampson, 1958 , A. oblanceolatus Drews & Sampson, 1958 , A. ornatus Drews & Sampson, 1958 and A. coachellensis Drews & Sampson, 1958 . In addition, they transferred Aleyrodes nigrans Bemis, 1904 to Aleuropleurocelus and provided a key and illustrations to the eight species known at that time. Tetralicia granulata Sampson & Drews, 1941 , Aleurotrachelus cecropiae Bondar, 1923 and Tetralicia rotunda Baker, 1937 were transferred to Aleuropleurocelus by Mound & Halsey (1978), Martin (2005) and Martin & Mound (2007) respectively. Since then, the following 21 new species in the genus have been published:

A. anahuac Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2018a. A. annonae Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2018b. A. bidentatus Sánchez-Flores & Carapia-Ruiz, 2018a .

A. caudatus Sánchez-Flores & Carapia-Ruiz, 2018a .

A. chamaedoreaelegans Sánchez-Flores & Carapia-Ruiz, 2018b .

A. eriogonum Carapia-Ruíz, 2020a .

A. fouquieriasplendens Carapia-Ruiz & Sánchez-Flores, 2019a .

A. guazumae Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2018b. A. guerrerensis Carapia-Ruíz & Sánchez-Flores in Sánchez-Flores et al., 2018c. A. hyptisemoryi Gill in Polaszek & Gill, 2011.

A. kobei Sánchez-Flores & García-Ochaeta in Sánchez-Flores et al., 2021. A. mexicanus Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2018a. A. mixtecus Carapia-Ruiz, 2020b .

A. nevadensis Dooley in Dooley et al., 2010.

A. palidonigrans Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2021. A. pallidus Carapia-Ruiz & Sánchez-Flores, 2019b .

A. petenensis Carapia-Ruiz & García-Ochaeta in Carapia-Ruiz et al., 2023 A. popocatepetl Carapia-Ruiz & Sánchez-Flores in Sánchez-Flores et al., 2022. A. pseudogranulata Carapia-Ruiz & Sánchez-Flores in Carapia-Ruiz et al., 2020c. A. sampsoni Sanchez-Flores & Carapia-Ruiz in Sanchez-Flores et al., 2020. A. xalapensis Sánchez-Flores & Carapia-Ruiz in Sánchez-Flores et al., 2018b.

Currently, the genus Aleuropleurocelus contains 33 New World species of which 19, 12, 1 and 1 species were described from Mexico, USA, Guatemala and Brazil, respectively. Of these, only Aleuropleurocelus abnormis ( Quaintance, 1900) is known to occur on avocado, and A. nigrans and A. ceanothi are the only species in the genus that have been found in or intercepted at the U.S. Ports of Entry on plant products originating from countries other than the Americas. Dubey (2021) reported the occurrence of A. ceanothi in Hawaii based on a single puparium collected by J.W. Dooley, and one record exists of A. abnormis that was intercepted at a U.S. port of entry from plant material originating from the Philippines. Records of the distribution of species in a country based solely on specimens intercepted at a ports of entry on plant material originating from that country may indicate the likelihood that the species is present in the country; however, the actual presence of the species in these countries needs to be verified by collections made within the country.

Synonymy of Tetralicia and Aleuropleurocelus

Drews & Sampson (1956) described the puparium of A. laingi , the type species, as being: “elliptical to broadly ovate in form; apparent margin only slightly irregular; true margin with teeth; dorsal ridge without papilla-like structures; median posterior deflection of transverse molting suture not reaching distal portion of first abdominal suture; vasiform orifice devoid of teeth; orifice surrounded by a sclerotized ring; operculum cordate or subcordate in form, almost or completely filling orifice; lingula hidden by operculum; outer portion of marginal band deflexed; posterior protuberance usually present. The two genera differ in that Tetralicia possesses the following characters which are not found in Aleuropleurocelus : teeth in the vasiform orifice, papilla-like structures on the dorsal ridge, true margin apparently smooth or only slightly irregular, transverse molting suture not reaching the distal portion of first abdominal suture vasiform orifice subcircular, and operculum shorter and smaller. The genera are similar in that both have the deflexed portion of the marginal band, a sclerotized ring surrounding the vasiform orifice, and the lingula hidden by the operculum”. In the key they provided, they focused on differences in two characters⸺in Tetralicia , the inner margin of vasiform orifice has teeth and the operculum fills not more than three-fourths of orifice; whereas in Aleuropleurocelus , the inner margin of orifice is smooth and the operculum fills or nearly fills the orifice. However, at that time (1956) Tetralicia only included the type species, T. ericae and Aleuropleurocelus only included A. laingi , A. ceanothi and A. sierrae . As more species of each genus have become available for study, the suite of separation characters has shown to be not entirely consistent and reliable.

The details of the true margin and vasiform orifice are often difficult to observe because of their very dark color and the descriptions of these characteristics in many species of the genera Aleuropleurocelus and Tetralicia are inadequate to confirm these differences among all species of the two genera. However, based on our review of all of the species currently placed in the two genera, the forementioned characters that Drews & Sampson (1956) used to separate the two genera vary and sometimes are found among species currently placed in either genus. For example, Tetralicia species are said to have the true lateral margin smooth or irregular without teeth, whereas in Aleuropleurocelus the true lateral margin is crenulate or toothed. However at least T. erianthi has a crenulate lateral margin and among Aleuropleurocelus species the lateral margin is highly variable, ranging from crenulate to having large, sometimes bifurcate teeth. In addition, the shape of the teeth along the lateral margin among species of other genera such as Aleurotrachelus Quaintance & Baker, 1914 is also highly variable. The vasiform orifice of Tetralicia species is said to be “toothed” internally (with ridges), whereas in Aleuropleurocelus , the inner margin of orifice is smooth. Although this is true for T. ericae (the type species), it is not true for all of the species currently placed in Tetralicia . The vasiform orifice of T. erianthi and T. debarroi is smooth and that of T. iberiaca is reticulate. The sides and floor of the vasiform orifice of Aleuropleurocelus species are usually smooth, however some species have ridges along the lateral margins. The operculum of Tetralicia species is said to fill or nearly fill the orifice, whereas in Aleuropleurocelus the operculum fills 0.6–0.9x the orifice. That appears to be true for all of the Tetralicia species as well as for many of the Aleuropleurocelus species ( Table 1 ) and thus cannot be considered as a valid character to justify maintaining them as separate and distinct genera.

In addition, we compared the chaetotaxy, presence or absence of eyes, and characteristics of the transverse molting suture and deflexed margin ( Table 1 ). All of the species currently placed in Tetralicia lack eyes and mesothoracic submedial setae (Ts2); the European and Australian species lack the metathoracic submedial setae (Ts3), all lack cephalic setae (except for T. erianthi which has 3 short pairs versus 1 pair in the Aleuropleurocelus species that have cephalic setae) and all of these have very short As8 and Cas setae. The two species from Chad ( T. graminicola and T. tuberculata ) have long Cs1, Ts3, As8 and Cas setae. In Tetralicia , the transverse molting suture (tms) reaches the submargin, except in T. ericae where it reaches the lateral margin and the lateral margin is deflexed only 0.2x the radius of the body (measured at the tms) in all Tetralicia species except T. ericae where it is deflexed 0.4x the radius. In Aleuropleurocelus , the eyes are present or absent, the Ts2 setae are present in 24 species and the Ts3 setae are present in 25 of the 32 species currently in the genus; however some species lack cephalothoracic setae entirely. The transverse molting suture (tms) is highly variable, reaching the submargin or the lateral margin, and the lateral margin may be deflexed 0.1–0.5x the radius. Therefore, since no characteristics were found that could clearly distinguish the two taxa, we propose that Aleuropleurocelus be considered a junior synonym of Tetralicia and all of its species transferred to the latter genus.

Origin of the genus Tetralicia

Although the genus Tetralicia was described from the Western Palearctic region, it appears that it may have originated in the Neotropical region based on the number and diversity of species and their hosts. Only three species have been described from the Western Palearctic region. Two of these species, T. ericae and T. iberiaca , have been found only on Erica ( Ericaceae ) in Europe and T. erianthi has been found only on Tripidium and Rununculus in Turkmenistan and Iran. The species from Australia, T. debarroi , differs greatly from the other species in the genus by its apparent lack of dorsal setae and being covered with tubercles ( Fig. 4A ). The other two species that have been placed in the genus, T. graminicola and T. tuberculata , have been found only in Chad on Hyparrhenia and Vitex , respectively. In contrast, the genus Aleuropleurocelus is very speciose and diverse in the New World with most of the species described from Mexico and the Southwestern USA on a variety of plant species.

Diagnosis of the genus Tetralicia

Puparium: venter smaller than dorsum, resulting in a deflexion of the dorsum, so that the true lateral margin is located underneath the dorsal surface; spiracular and caudal cleft or pores absent, teeth along lateral margin not differentiated at the tracheal or caudal openings; puparia black and heavily sclerotized in most species, rarely pale (only in T. pallidus , T. palidonigrans and T. tuberculata ); submarginal ridge absent; vasiform orifice slightly elevated, sometimes appearing to be surrounded by a sclerotized ring, variously shaped with operculum most commonly filling the orifice; lingula usually concealed by operculum; transverse molting suture reaching to submargin or lateral margin; prothoracic (Ts1) setae absent; cephalic setae (Cs1), mesothoracic (Ts2) and metathoracic (Ts3) setae present or absent; first abdominal setae (As1) absent; one pair of anterior marginal setae (ams) and posterior marginal setae (pms) present; caudal protuberance developed or undeveloped; eyes present or absent. Tetralicia is similar to Aleurovitreus Martin, 2005 a Neotropical genus which also has a deflexed lateral margin and similar dorsal chaetotaxy (Ts1 and As1 absent); however, all of the species in the latter genus are primarily pale, some having brownish or blackish patches, the puparial cuticle is much smoother and finer, the venter less robust, the dorsum of most of the species is covered with duplex geminate pores on sclerotized areas, and is without evident waxy secretions in nature. Tetralicia is also similar to Aleuroplatus in color (the majority of species in both genera are black), the lack of a submarginal ridge and As1 setae, but differs from that latter genus which does not have the lateral margin deflexed and the tracheal and caudal openings are slightly differentiated from the lateral margin in most species.

Adults: The adults of most of the species in the two genera are not well known and have not been illustrated except for that of the type species, T. ericae for which Bink-Moenen (1989) provided illustrations of the male and female antennae and genitalia ( Fig. 3 ). Based on these illustrations and an examination of adults of T. ericae in the USNM collection, the antennae of both the male and female have the 2 round sensoriae towards the apex of the third antennal segment (F3) and the males have an additional elongate sensorial cone arising towards the apex in some specimens and a pair of long sensorial cones arising towards the middle of the segment; the fourth segment (F4) is very short, transverse to less than 2x as long as wide without sensoriae; the fifth segment (F5) is long, about 5–6x as long as wide, without sensoriae in the female and with a long basal cone sensorium in the male, which is unusual in the male whiteflies that are known; the sixth segment (F6) is short, about 2x as long as wide and without sensoriae in the female and some males with a short cone sensorium; the seventh segment (F7) is elongate, wide basally and tapering to a long point apically with a round sensorium basally at the point where it tapers, some males with a long sensorial cone at the base. The hind tibiae have a comb of about 18 setae and lack a brush (without two or more setae close together on the margin). The ovipositor of the female is very elongate with long stylets, the male claspers lack teeth on the inner margin and have a long apical projection and the aedeagus is sigmoid. The antennae of the adults of T. sawyeri n. sp. ( Figs. 8B–8C ) have the third flagellar segment (F3) elongate with a round sensorium at the apex, another subapically and a long, rod-like sensorial cone arising in the distal third of the segment; F4 segment more elongate (more than 2x as long as wide) without sensoriae; F5 elongate with a round sensorium apically; F6 more elongate, about 3x as long as wide and with a round sensorium; F7 elongate with a longer basal part, tapering distally and with a round sensorium at the base of the tapered part. The hind tibia has a comb of about 18 setae and a brush consisting of 2 setae. The ovipositor is not as elongate as that of T. ericae ( Fig. 8G ).

Keys and characters of Tetralicia species

Bink-Moenen (1983) provided a key to the two species of Tetralicia from Chad; no other keys exist for species currently in the genus Tetralicia . Drews & Sampson (1958) provided the first key to Aleuropleurocelus species including 8 species known at that time. Sánchez-Flores & Carapia-Ruiz (2018c) provided a key to 9 species of Aleuropleurocelus having an oval shaped body and later Sánchez-Flores et al. (2021) provided a key to 10 species of Aleuropleurocelus having an oval to round shaped body. Sanchez-Flores et al. (2020) erected the Aleuropleurocelus ceanothi group, which they defined as species in which the transverse molting suture of the puparia extends to the submargin and provided a key to 7 species in the group.

The puparia of almost all of the species are black making it difficult to see and evaluate the morphological characters and much needs to be learned regarding which characters are stable for each species and the degree of intra- and interspecific variation that occurs in the genus. From our observations and review of the literature, we consider the number and position of the dorsal setae in the puparium of a given species to be stable characters. Note that oftentimes the dorsal setae are broken off during specimen preparation, but their presence can be discerned by the paired setal bases which remain in the position of these setae. The setal complement of earlier instars may vary from that of the puparium; Sánchez-Flores et al. (2022) reported that the cephalic setae of A. popocatepetl were absent in the puparium but present in the third instar nymph. The length and shape of the dorsal setae appear to be somewhat stable, however they have been shown to vary depending on the characteristics of its host and other environmental factors in other aleyrodine genera, and therefore should be approached with caution. The body shape is given as the ratio of the length of the body versus its width measured along the tms. Although, this ratio may vary somewhat, it is considered to be a fairly stable character. Coloration appears to be stable in the species that have dark puparia; however earlier instars may be entirely or partially pale. The degree to which the tms extends to the lateral margin and characteristics of the vasiform orifice appear to be a consistent characters. We have included host and distribution information and illustrations for all of the species in the key. All measurements of the setae are given in µm when available. The habitus of all described species are illustrated ( Figs. 3–6 ), most of them modified from those found in the original publications; however, some were taken of specimens in the USNM collection (see checklist for sources).

Tetralicia species of the world

Information on the taxonomy, hosts, distribution and natural enemies of the Tetralicia species of the world is provided in the annotated checklist below, followed by an illustrated key to the species of the world. All of the species currently in Aleuropleurocelus (a masculine gender genus) are transferred to the genus Tetralicia (a feminine gender genus); the species epithets of several of the species have been changed to reflect the change of gender. Distribution records of species in countries known only from specimens intercepted at a U.S. Port of Entry are followed by the abbreviation [int].

Figures

FIGURE 3. Tetralicia ericae Harrison, 1917. (A–E) puparia: A) habitus drawing, B) habitus slide specimen, C) abdomen, D) vasiform orifice slide specimen, E) vasiform orifice drawing; (F–K) adult male: F) habitus, G–H) genitalia, I–K) antennae; (L–P) adult female: L) habitus, M–N) ovipositor; O–P) antennae. Sources: A, E, H, I, J, N (Bink-Moenen, 1989); B, C, D, F, G, K, L, M, P (USNM specimen).

FIGURE 4. Puparia of Tetralicia species. A) debarroi Martin & Carver, B) erianthi Danzig, C) graminicola Bink-Moenen, D) iberiaca Bink-Moenen, E) tuberculata Bink-Moenen, F) cecropiae (Carapia-Ruiz, 2020b) G) cecropiae Bondar (type, MZU), H) cecropiae (type, USNM), I) cecropiae (type, Bondar 1923).

FIGURE 8. Tetralicia sawyeri n. sp. A) adults on avocado leaf; B–H) adult female: B) antenna, C) antenna, F3–F7 =flagellar segments 3–7, rs=round sensoriae, sc=sensorial cone, D) tibia I, E) tibia II, tb=tibial brush, F) tibia III, tc=tibial comb, G) ovipositor, ov=ovipositor, H) cg=cement gland.