Pseudophilothrips gandolfoi, Mound & Wheeler & Williams, 2010

Mound, L. A., Wheeler, G. S. & Williams, D. A., 2010, Resolving cryptic species with morphology and DNA; thrips as a potential biocontrol agent of Brazilian peppertree, with a new species and overview of Pseudophilothrips (Thysanoptera), Zootaxa 2432 (1), pp. 59-68 : 62-66

Pseudophilothrips gandolfoi sp.n.

Male macroptera. Body blackish brown with red hypodermal pigment; antennal segment III sharply yellow ( Fig. 4 ), IV with variable paler marking, II with apex pale; fore tibiae and fore tarsi also with small paler areas, hind tibiae and tarsi as dark as body; fore wing shaded around sub-basal setae with shaded area extending medially at least half-way along wing; all major setae dark, including those on tergite IX. Antennae 8-segmented, VIII slightly constricted at base, III with one slender sensorium, IV with three sensoria. Head elongate ( Fig. 8 ), fore ocellus projecting over bases of antennae, cheeks weakly constricted medially, strongly constricted near base; maxillary stylets retracted almost to level of postocular setae, less than 0.2 of head width apart medially; postocular setae about as long as dorsal eye length, apices blunt to sub-acute; mid-dorsal setae usually no longer than diameter of an ocellus (one paratype male with one of these setae stout but short). Pronotum ( Fig. 7 ) with all 5 pairs of major setae developed but variable in length; anteromarginal and midlateral setae sometimes longer than anteroangulars; posteroangular setae sometimes as long as median length of pronotum, usually shorter; epimeral setal pair II varying from no longer than width of base of a major seta to stout and 0.5 as long as epimeral setal pair I. Fore tarsus with no tooth. Metascutum with median setae small ( Fig. 7 ), usually no sculpture present between bases of these setae. Prosternal basantra not developed, mesopresternum transverse but slightly narrowed medially; metathoracic sternopleural sutures scarcely developed. Fore wing sub-basal setae long with apices blunt; duplicated cilia varying in number 13– 18. Pelta triangular with wavy margins ( Fig. 9 ); tergite IX with three pairs of major setae all almost as long as tube.

Measurements (male holotype in microns). Body length 3000. Head, length 300; median width across cheeks 200; postocular setae 100. Pronotum, length 155; median width 320; major setae am 50, aa 50, ml 55, epim 125 (40), pa 110. Metanotal median setae 35. Fore wing, length 1150; sub-basal setae 80, 90, 100. Tergite IX setae, S1 280; S2 250; S3 300. Tube length 310. Antennal segments III–VIII length 100, 85, 80, 75, 70, 40.

Female macroptera. Similar to male but often larger with longer setae.

Measurements (large female paratype in microns). Body length 3350. Head, length 330; median width across cheeks 220; postocular setae 170. Pronotum, length 180; median width 380; major setae am 80, aa 50, ml 100, epim 190 (60), pa 130. Metanotal median setae 40. Fore wing, length 1350; sub-basal setae 110, 140, 130. Tergite IX setae, S1 320; S2 350; S3 300. Tube length 320. Antennal segments III–VIII length 110, 90, 85, 80, 80, 45.

Larvae. Body colour deep crimson red ( Fig. 2 ), in contrast to the orange larvae of P. ichini ( Fig. 3 ).

Material studied. Holotype male, BRAZIL, Parana, Curitiba, from Schinus terebinthifolius , iv.2008 (G.Wheeler), in United States National Museum of Natural History , Washington.

Paratypes: 4 females 6 males collected with holotype [and 3 red larvae] ; 11 females 21 males reared on same host plant under quarantine in Florida from specimens collected at Curitiba (including 2 males from which DNA was obtained) .

Paratypes deposited in Departamento Entomologia, ESALQ / USP, Piracicaba; USNM, Washington; Entomology Department, University of California, Riverside ; Natural History Museum , London ; Senckenberg Museum , Frankfurt ; Australian National Insect Collection , Canberra .

Comments. There seems to be only one non-varying structural character by which adults of this new species can be distinguished from P. ichini . In all the available specimens the metanotal median setae are shorter than the fore wing sub-basal setae S1 and slender, whereas in ichini the metanotal setae are usually stout ( Fig. 6 ) and always longer than the fore wing sub-basal setae S1. In addition, both sexes of ichini from all sites usually have the mid-dorsal pair of setae on the head stout and about half as long as the major postocular setae, although almost 5% of the available specimens have one or both of the mid-dorsal setae minute and thus share this character state with the new species. Antennal segments III and IV are generally less slender in the new species than in ichini , but vary in both species in relation to body size. Other characters are also too variable to provide easy discrimination between the two species.

In both species, the lengths of the major pronotal setae are particularly variable, both within and between the sexes, thus obscuring any inter-specific differences. Moreover, bilateral asymmetry in the lengths of major setae, including those on the pronotum, is common in both species. This variation has clear implications for distinguishing species in this genus when they are known only from small samples. In contrast, the difference in colour between the larvae of the two species, orange in ichini but deep crimson red in gandolfoi , is very distinctive.

The systematics of Pseudophilothrips

The family Phlaeothripidae , to which this new species belongs, comprises two sub-families, but the suprageneric classification of the largest of these, the Phlaeothripinae, is not satisfactory. Currently, most of the leaf-feeding species in this sub-family are referred to the “ Liothrips -lineage”, a poorly defined group ( Mound & Marullo, 1996) that includes several hundred species in about 100 genera, of which 40 are associated with leaf galls ( Mound, 1994). The genus Liothrips itself includes 250 species worldwide, but many of these are known only from one or very few specimens ( Mound & Pereyra, 2008). As a result, there are few wellestablished host-plant associations for the species, and almost no studies on the structural variation that might be expected within and between populations. For the purposes of the present study, original specimens of most of the species of Liothrips described from North and South America have been re-examined during visits to the major museum collections in Frankfurt, London, Washington and California. As a result several members of Liothrips are here transferred to Pseudophilothrips , and the definition of this genus is reexamined.

Johansen (1979) erected Pseudophilothrips for a single new species, P. moundi , based on eight females and four males taken from an unidentified tree in Vera Cruz State, Mexico. Shortly after this, the same author (1981) described a second species in this genus, P. amabilis , based on a single female from northern Mexico, and he also included in the genus the species Liothrips ichini Hood. The only character used to define Pseudophilothrips was the presence on the head of four long postocular setae, in contrast to the normal condition amongst Phlaeothripidae of only two such setae. Despite this, the only specimen of P. amabilis was illustrated as having one of the four postocular setae very short, and Johansen (1981) also stated that P. ichini sometimes has the inner pair of these setae short. The genus was thus not clearly distinguished from the worldwide genus Liothrips . Mound & Marullo (1996) recognized this problem and, in transferring a fourth species into Pseudophilothrips , they proposed distinguishing the genus on the following character states:

1. Males with major setae pair S2 on tergite IX as long as pair S1;

2. Head long with slightly concave cheeks;

3. Head sometimes with two pairs of postocular setae

4. Pronotal epimera sometimes with two pairs of major setae.

Character state 1 is the most constant of these, although even this is variable within one species, P. didymopanicis (see below). The second character state cannot be considered valid; to a large extent it correlates with body size, and it recurs in various species of Liothrips around the world. The third and fourth character states are variable, both within and between species, but they do not occur in any of the numerous Old World species of Liothrips . Thus Pseudophilothrips apparently represents a discrete New World, mainly South American, lineage. Despite this, there is no evidence that it is sister-group to the larger genus, and presumably it was derived from within Liothrips . The following 13 species are here included in this genus.

Pseudophilothrips amabilis Johansen, 1981 . This species is known only from the description based on a single female from Mexico.

Pseudophilothrips adisi ( zur Strassen, 1978) comb.n. Described from Brazil in Liothrips , and known as a pest of Paullinia cupana (Sapindaceae) , this species possesses character states 1 and 4 above, but there is only one pair of postocular setae, and the head is not elongate. One male in the type series has one of the two metanotal setae unusually stout, although the left seta of the pair is short as in the rest of the type specimens.

Pseudophilothrips avocadis ( Hood, 1935) comb.n. Described in Liothrips and known from Panama and Costa Rica in association with Persea americana (Lauraceae) , this species possesses character state 1 above, and has a long head, but has only a single pair of postocular and epimeral setae.

Pseudophilothrips didymopanicis (Del Claro & Mound, 1996) comb.n. Described in Liothrips from Brazil on Didymopanax (Araliaceae) , this species possesses character states 1 and 3 above, although both are variable (even bilaterally asymmetric) among the available specimens. There is only one pair of setae on the prothoracic epimera, and the head is not elongate.

Pseudophilothrips fugitivus ( Johansen, 1983) . Described in Phrasterothrips from 20 specimens taken on an unknown tree, this Mexican species was later transferred to Pseudophilothrips by Mound & Marullo (1996). It possesses character states 1 and 4, but the long head is reported to have only one pair of postocular setae.

Pseudophilothrips gandolfoi sp.n. Known only from Curitiba in southern Brazil on Schinus terebinthifolius .

Pseudophilothrips ichini ( Hood, 1949) . Described in Liothrips , this species was referred to Pseudophilothrips by Johansen (1981). The original specimens came from Rio de Janeiro, but the species is widespread in eastern Brazil on Schinus terebinthifolius (Anacardiaceae) .

Pseudophilothrips moundi Johansen, 1979 . Described from 12 specimens from an unknown tree, this Mexican species is reported as having character states 1, 2 and 3, but not 4.

Pseudophilothrips obscuricornis ( Priesner, 1921) comb.n. Described as a variety of Liothrips seticollis , this species was based on a single male from Paraguay that exhibits character state 1 above. This slidemounted specimen, with only one antenna, has been re-examined on loan from the Museum für Naturkunde, Berlin. Antennal segment III is yellow, but segments IV–V are yellowish-brown. The metanotal median setae are small, and the setae on tergite IX are rather paler than the setae on tergites VII–VIII. This species is interpreted here as the same as a species that has been collected fairly commonly (by Estevão A. Silva) on the leaves of Banisteriopsis malifolia [ Malpighiaceae ] at Uberlândia, M.G., Brazil. In these specimens, the metanotal setae are larger than in the male from Paraguay, but vary in size, and the setae on tergite IX also vary from light to dark brown.

Pseudophilothrips perseae ( Watson, 1923) comb.n. Described in Liothrips and known only from Guatemala and Honduras in association with Persea (Lauraceae) , this species is very similar to P. avocadis , but has the antennae more extensively yellow.

Pseudophilothrips retanai Soto, 2000 . Known only from two males taken in a trap in Costa Rica, this species has character states 1, 3 and 4 above, but was described as having antennal segments III–V pale yellow, and segment VI yellow at the base.

Pseudophilothrips seticollis ( Karny, 1912) comb.n. Described in Liothrips , and known only from the few original specimens from Paraguay, this species possesses character state 1, but antennal segment III is yellow, IV shaded at only at the apex, V is yellow in the basal fifth, and VI is yellow at the base.

Pseudophilothrips varicornis ( Hood, 1912) comb.n. Described in Liothrips , and studied from California, Mexico, Bahamas, Hawaii, and Tahiti, this species is associated with the leaves of various Malvaceae . It possesses character states 1 and usually 4, but the second pair of epimeral setae varies in development in both sexes.

Considering these 13 species, five of them are known to have antennal segments III and IV more or less equally yellow: amabilis, didymopanicis, perseae , retanai and seticollis . In contrast the other eight species have these two antennal segments differing sharply in colour; III is yellow, but IV largely dark brown. Unfortunately, obscuricornis is variable and intermediate between these two groups, and presumably is closely related to didymopanicis . Two of the eight species have the major setae on tergite IX distinctively pale, often almost white ( avocadis, varicornis ), whereas the other six species are considered to have these setae about as dark as the setae on the other tergites. One of these, adisi , has the head unusually short, less than 1.1– 1.2 times as long as the maximum width, whereas the head is considerably longer (1.4 times) among the remaining five species. The type species of the genus, moundi , is illustrated ( Johansen, 1981) as having postocular setae considerably shorter than the dorsal length of a compound eye, whereas these setae are long and slender in the remaining four species. The Mexican species fugitivus is reported to lack a second pair of major postocular setae, and to have the median metanotal setae long and stout. From the original description, it seems possible that this species may represent a northern race of ichini , but this requires further study.

In conclusion, it is clear from both the morphological and the molecular character states, that the concept of species in this genus is particularly difficult to define. Biological studies on the forms associated with Schinus suggest that there is likely to be a high degree of host specificity among Pseudophilothrips species , but that this may not always be closely correlated with structural or colour differences. The phenomenon, and taxonomic problem, of sibling species is probably widespread amongst leaf-feeding Phlaeothripidae of the Liothrips group, as is also clear from combined morphological and molecular studies on Australian leafgalling thrips ( McLeish et al., 2006). This problem at species level is further reflected in the difficulties of assessing systematic relationships. The genus Liothrips occurs world wide, and the many species included exhibit a considerable range of body form. Morphological studies have failed to recognize useful segregates within this complex, with the exception of the group discussed in this paper. It is to be hoped that future molecular studies may provide data less susceptible to homoplasy than character states like setal lengths, and head length/width ratios. A similar problem exists with the species allocated to Teuchothrips , a particularly poorly defined genus used primarily for Australian species in the Liothrips complex (Mound, 2008).

Figures

FIGURES 1–4. Pseudophilothrips from Schinus terebinthifolius. (1) colony of adults inducing leaf distortion. (2) P. gandolfoi red larvae. (3) P.ichini orange larvae. (4) P. gandolfoi holotype antenna.

FIGURES 6–9. Pseudophilothrips species. (6) P. ichini pronotum and metanotum. (7) P. gandolfoi pronotum and metanotum. (8) P. gandolfoi holotype head and pronotum. (9) P. gandolfoi holotype pelta and tergites II–III.