Trioza turouguei sp. nov. (Hemiptera, Psylloidea, Triozidae), a new psyllid species from Taiwan inducing pea-shaped stem galls on Cinnamomum osmophloeum (Lauraceae), with notes on its galling biology

Abstract Trioza turougueisp. nov., a new species of jumping plant lice (Hemiptera, Triozidae) from Taiwan, is described and illustrated based on adults and immatures. The latter induce pea-shaped galls on the stems of Cinnamomum osmophloeum Kaneh. (Lauraceae). The gall phenology of the new species is described. A list of species of Triozidae associated with Cinnamomum in the Old World is provided. The following nomenclatorial acts are proposed: Trioza inflata Li, 1992 = Trioza xiangicamphorae Li, 1992, syn. nov.; Siphonaleyrodes formosanus Takahashi, 1932, stat. rev., is removed from synonymy with Trioza cinnamomi (Boselli, 1931).


Introduction
Jumping plant lice or psyllids (Hemiptera, Sternorrhyncha, Psylloidea) are phloemfeeding insects that are highly host specific, especially during the immature stages (Hodkinson 1974). The superfamily is comprised of approximately 4,000 species in more than 200 genera worldwide (Li 2011;Burckhardt and Ouvrard 2012;Ouvrard 2020). Closely related psyllid species tend to develop on closely related plant species (Burckhardt and Basset 2000;Percy et al. 2004;Ouvrard et al. 2015;Burckhardt and Queiroz 2020). As other phytophagous insects, many psyllids are gall inducers, particularly those of the families Triozidae, Phacopteronidae, and Calophyidae (Burckhardt 2005;Malenovský et al. 2007;Yang and Raman 2007). Psyllid galls are characterized by a very specific morphology, formation site, and restriction to a single or a few related plant species (Hodkinson 1984;Burckhardt 2005).
The first studies on the psyllid fauna of Taiwan are from foreign researchers made during the first half of the 20 th century (Kuwayama 1908(Kuwayama , 1910(Kuwayama , 1931Enderlein 1914). Half a century later, Yang (1984) published the first comprehensive monograph, which was subsequently supplemented and expanded (Fang and Yang 1986;Yang et al. 1986;Lauterer et al. 1988;Fang 1990;Yang et al. 2004Yang et al. , 2009Yang et al. , 2013Liao et al. 2016;Liao and Yang 2018;Cho et al. 2020). According to these studies, more than half of the Taiwanese psyllid species are gall inducers and several of these are associated with the Lauraceae (Yang et al. 2006), a family of Magnoliids, an early branch in the angiosperm tree. Hollis and Martin (1997) compiled a list of the known psyllids associated with Lauraceae and recorded ten species developing on the lauraceous genus Cinnamomum in the Oriental realm.
Cinnamomum osmophloeum Kaneh. is a tree species endemic to Taiwan, growing at low elevations around the island. The tree species has some economic potential for its essential oils in the leaves (Chang et al. 2001), which are similar to those found in the bark of Indonesian cassia (Cinnamomum burmanni (Nees & T. Nees) Blume) with antibacterial, carminative, and anti-fungal properties. On the stems of C. osmophloeum, peashaped closed galls were found, in the field as well as on herbarium specimens in Taiwan, which are induced by an undescribed psyllid species. According to Hodkinson (1984Hodkinson ( , 2009, stem galls induced by psyllids are relatively rare compared to the much more common leaf galls. For this reason, also little is known about the phenology of stem galls.
Here, we formally name the species on C. osmophloeum as Trioza turouguei sp. nov., describe its adults and immatures, discuss its relationships to other psyllids developing on Cinnamomum, and provide information on the life cycle and gall phenology.

Materials and methods
Psyllids were collected by sweeping and directly searching on Cinnamomum osmophloeum. The material is dry mounted or preserved in 70% and 99% ethanol. Some specimens were cleared in 15% potassium hydroxide and examined in orange oil or glycerol or permanently mounted in Canada balsam on a slide. Information on galls was taken in the field and from herbarium specimens.
Photographs of most morphological characters were taken with a compound microscope (Leica DM 750) equipped with a digital camera (Canon EOS 600D). Images of the forewings of adults were taken with a stereomicroscope (Leica MZ 125) equipped with a digital camera (Olympus EP-1). The photographs were montaged using focus stacking software (Helicon Focus, Helicon Soft). The morphological terminology follows White and Hodkinson (1982), Ossiannilsson (1992), Hollis (2004) and Yang et al. (2013).
The life cycle and gall phenology were observed at the Huisun Experimental Forest Station (24°05'24"N, 121°02'03"E; 660-370 m a.s.l.) from January to December 1996. We selected eight trees of C. osmophloeum to record the phenology of the plants and the galls induced by T. turouguei sp. nov. The terminology of gall development follows Lalonde and Shorthouse (1984) and Rohfritsch (1992). The stage of immatures inside the gall was checked by dissection of the gall.  almost straight anterior margin; apex pointed. Distal segment of aedeagus shorter than paramere, apical third inflated, spoon-shaped. Female proctiger truncate apically.
Structure. Body large, length from anterior head margin to tip of folded forewing 5.4-6.8 mm; covered in long fine setae. Head ( Fig. 2A) nearly as wide as thorax, inclined in a 45° angle from longitudinal body axis. Vertex 1.8-2.0 times as wide as long, moderately concave at posterior margin. Genal processes prominent, 0.8-1.0 times as long as vertex along mid-line, divergent, conical, blunt at apex, pubescent. Antenna ( Fig. 2B) slender, 10-segmented, 1.5-1.8 times as long as head width, relative length of flagellar segments as 1.0: 0.4: 0.3: 0.4: 0.3: 0.3: 0.2: 0.2, with a single rhinarium on each of segments 4, 6, 8 and 9; longer, pointed terminal seta 1.1 times and shorter, truncate terminal seta 0.2 times as long as segment 10. Thorax weakly arched dorsally. Pronotum deflexed from mesothorax in a 45° angle. Legs slender. Meracanthus well developed, horn-shaped, acute at apex (Fig. 2C); metatibia 0.9-1.2 times as long as head width, slightly inflated basally with four or five small spines, with 1+2 or rarely 1+3 apical spurs. Forewing (Fig. 2D) 5.4-6.4 times as long as head width, 2.5-2.7 times as long as wide, widest slightly distal to the middle; wing apex subacute, lying in cell m 1 near apex of vein M 1+2 ; vein R+M+Cu strictly trifurcating into veins R, M and Cu; vein Rs moderately long, irregularly, concavely curved to fore margin of wing; vein M weakly curved with very long diverging branches; cell m 1 large; vein Cu 1a strongly curved in the basal third; cell cu 1 smaller than cell m 1 ; line connecting apices of veins Rs and Cu 1a distal of bifurcation of vein M; surface spinules absent except for base of cell cu 2 ; radular spinules present along wing margin in the middle of cells m 1 , m 2 and cu 1 . Hindwing 0.7 times as long and 0.5 times as wide as forewing; costal margin with five or six setae proximal to costal break, setae distal to costal break clearly divided into two groups. Abdominal tergites glabrous except for a lateral row on either side of tergite 2 in male and tergite 3 in female.
Male terminalia ( Fig. 3A-C). Proctiger tubular, in profile broadly convex posteriorly, covered in long setae except for basal third laterally (Fig. 3A). Subgenital plate subglobular, with long setae laterally and ventrally; dorsal margin angular in basal third. Paramere (Fig. 3B) about as long as proctiger; in profile lamellar, irregularly narrowing to apex which is acute and weakly directed anteriad; outer face glabrous except for margins and apex; inner face beset with long setae mostly along fore and hind margins as well as basally. Distal segment of aedeagus (Fig. 3C) shorter than paramere, apical third inflated, spoon-shaped; sclerotized end tube of ductus ejaculatorius short, sinuous. Female terminalia (Fig. 3D) cuneate, short. Proctiger with straight dorsal margin and blunt apex, as long as subgenital plate; with a transverse row of long setae in the middle and long setae apically; circumanal ring one third as long as proctiger,  consisting of two unequal rows of pores (Fig. 3E). Subgenital plate, in profile, irregularly triangular, acute at apex; beset in long hairs laterally and ventrally. Dorsal valvulae cuneate, ventral valvulae straight lacking teeth.

Fifth instar immatures
Measurements (range, mean ± SD) in mm (5 immatures Etymology. Named after the Chinese common name of the host plant, 土肉桂, transliterated as "turouguei"; to be treated as a noun in the nominative singular standing in apposition. Distribution. Taiwan. Host plant and its phenology. Cinnamomum osmophloeum Kaneh. (Lauraceae). Leaf and flower buds of C. osmophloeum appear in late April. Young leaves grow from late May to late June and flowers bloom from early June to August. Fruits ripen from September to November.
Biology. Trioza turouguei sp. nov. is univoltine and induces pea-shaped galls (Fig. 5C, D) on the stems of new shoots of C. osmophloeum. The galls are unilocular with a single immature in each chamber. The annual life cycle of the gall is synchronized with the host phenology and passes through the following four stages of development as defined by Rohfritsch (1992). (1) Initiation: this stage is very short lasting from late April to the early May. After the first instar inserts its stylets into the phloem and injects saliva, the area on which it sits, either a flower, or leaf petiole, or a tender stem, transforms into a tiny pit and the surrounding area starts swelling. (2) Growth and differentiation: from late May to November, the gall forms and completely covers the immature. The second instar appears in late May and lasts until September. The third and fourth instars can be found in October and November, respectively. (3) Maturation: in December, the gall enters the maturation stage, and the immatures attain the final (fifth) instar. The gall reaches its maximum size with a diameter/length of 5.0/7.8 mm. (4) Dehiscence: during January and March, the gall dehisces by mechani- cal force in the gall tissue. The final instar immatures crawl out of the gall where the adults emerge. Soon after, the adults start mating.
Affinities. Hollis and Martin (1997) listed ten named triozid species from the Old World and one undescribed Trioza species from the New World associated with Cinnamomum spp. An updated list of the Old World species is provided in Table 1, taking into account taxonomical changes of the last 20 years including some proposed here. Despite a certain morphological resemblance among the Old World species, it is questionable if the group is monophyletic. The species share (mostly) following characters: genal processes developed, more than half vertex length; antennal segment 3 very long (not in T. hangzhouica (Li, 1994)); terminal antennal setae strongly unequal in length; forewing transparent, with short concave or sometimes sinuous vein Rs; hindwing over half as long as forewing; metatibia with a group of basal spines and 1+2 small apical spurs (1+3 in T. exoterica Yang, 1984 andT. nigricamphorae Li, 1993). Li (2005Li ( , 2011 erected two ill-defined, probably polyphyletic genera Triozopsis (type species Trioza nigricamphorae) and Metatriozidus (type species Metatriozidus ileicisuga Li, 2011) in which he also placed species associated with Cinnamomum. Here we adopt the broad concept of Trioza Foerster by Hollis (1984) and consider Metatriozidus and Triozopsis as subjective synonyms following Yang et al. (2013).
Based on the examination of relevant types (CAUB) we propose here following new synonymy: Trioza inflata Li, 1992, = Trioza xiangicamphorae Li, 1992, syn. nov. Mound and Halsey (1978 transferred Siphonaleyrodes formosanus Takahashi, 1932 from whiteflies to psyllids and synonymised it with Trioza cinnamomi (Boselli, 1931). According to the original description, the immatures of S. formosanus are relatively slender and possess several rows of marginal sectasetae (Takahashi 1932). Immatures of T. cinnamomi on the other hand are broader and possess only a single row of marginal sectasetae (Miyatake 1969;NHMB data). Based on this evidence, we conclude that the two taxa are not conspecific and remove the former from synonymy with Siphonaleyrodes formosanus, stat. rev. The species is currently only known from immatures which makes it difficult to place this genus within the current classification of Triozidae  (Burckhardt andOuvrard 2012, Percy et al. 2018). The type material of S. formosanus is apparently lost (M. M. Yang, pers. obs.). Trioza turouguei sp. nov. differs from the other species associated with Cinnamomum as indicated in the following keys. In particular, it is diagnosed by details of the male and female terminalia and the multilayered circumanal ring in the immature. Genal processes about as long as vertex along midline. Discussion and conclusions Hollis and Martin (1997) showed that sap sucking insects colonized Lauraceae more successfully than chewing insects by an order of magnitude of percentage of number of species associated with this family. The reason may be the phytochemicals in the leaves deterring chewing insects more efficiently than sucking insects. Among psyllid host plant families, Lauraceae is ranked 7 th in terms of number of associated psyllid genera (Ouvrard et al. 2015). More than two thirds of the psyllid species associated with Lauraceae belong to the Triozidae and of these almost two thirds induce galls or other deformations on their hosts (Hollis and Martin 1997). The Old World triozids developing on Cinnamomum (Table 1) fit this pattern. Of the 14 species, five with confirmed hosts (hosts marked with asterisk in Table 1) induce galls. Of the remainder, the association with Cinnamomum of seven species is likely but that of two (Trioza exoterica, T. hangzhouica) is questionable. The former develops on Cryptocarya chinensis (host confirmed by the presence of immatures) and Cinnamomum porrectum may be just casual plant (Burckhardt et al. 2014). The same is true for T. hangzhouica. Among the five species with confirmed hosts, all are monophagous except for T. cinnamomi which is narrowly oligophagous.
Cinnamomum osmophloeum, the host of Trioza turouguei sp. nov., has a scattered distribution in Taiwan growing in broad-leaved forests. Its conservation status is "Vulnerable" in the International Union for Conservation of Nature (IUCN) Red List (Pan 1998). This plant species is not hard to find at low to medium mountain areas in Taiwan, but the majority of trees are planted and only a few grow naturally. The unintentional introduction of Cinnamomum burmannii into Taiwan may endanger the natural population of C. osmophloeum (Tseng et al. 2008). Contrary to its host, adults, and galls of Trioza turouguei were found only in central Taiwan. Adults of Trioza turouguei are quite big and the galls are conspicuous on a plant species of medicinal interest. It is, therefore, surprising that the species has not been described before. One reason for this may be the very short period of adult emergence (1-2 weeks). Another reason is certainly that psyllid diversity in general, and that of the tropics in particular, is still insufficiently known.