Holopothrips diversity-a Neotropical genus of gall-inducing insects (Thysanoptera, Phlaeothripidae) Author Lindner, Mariana F. Author Ferrari, Augusto Author Mound, Laurence A. Author Cavalleri, Adriano text Zootaxa 2018 2018-10-04 4494 1 1 99 journal article 29290 10.11646/zootaxa.4494.1.1 ceb3ba80-3c38-4d93-97f1-ee98e52d1204 1175-5326 1445182 872F6F63-26E4-4CEC-B0EC-106B96D693FD Holopothrips Hood Holopothrips Hood, 1914 :49 (type species: Holopothrips signatus Hood, 1914 , by original designation). Phrasterothrips Priesner, 1921 :210 (type species: Phrasterothrips conducans Priesner, 1921 , by monotypy). Synonymised by Mound & Marullo, 1996 :289 . Diploacanthothrips Moulton, 1933 :239 (type species: Diploacanthothrips fuscus Moulton, 1933 , by monotypy). Synonymised with Phrasterothrips , by Priesner, 1949 :127 . Homorothrips Hood, 1954 :52 (type species: Homorothrips erianthi Hood, 1954 , by monotypy). Synonymised by Mound & Marullo, 1996 :289 . Anoplothrips Hood, 1954 :53 (type species: Anoplothrips jaboticabae Hood, 1954 , by monotypy). Synonymised by Mound & Marullo, 1996 :289 . Caraibothrips Bournier, 1993 :234 . (type species: Caraibothrips inquilinus Bournier, 1993 , by monotypy). Synonymised by Mound & Marullo, 1996 :289 . Type species: Holopothrips signatus Hood, 1914 : 50 . Diagnostic features: the following characters are those most frequently mentioned as diagnostic for this genus: presence of a third pair of wing-retaining setae on abdominal tergites II–VII, presence of anterior discal setae on metanotum, and males with multiple and complex pore plates ( Mound & Marullo 1996 ); visible and welldeveloped female spermatheca ( Zamora et al. 2015 ). However, variations of one or more of these traits are not uncommon within Holopothrips , with some members being included in the genus even when lacking one of the diagnostic features, due to sharing other morphological similarities or habits. All members of the genus have antenna 8-segmented; fore tibia unarmed; wings well-developed and fore wings bearing duplicated cilia; no sexual dimorphism in external characters has been observed in any Holopothrips species. However, other features, such as presence of three sense cones on antennal segments III–IV, large and bulbous eyes, association to galls, have been proposed as common within the genus, but are of limited use for diagnosing membership of Holopothrips . Several other morphological characters, such as body size, colouration, chaetotaxy, are highly variable within the genus, as described below. Morphological variation . Colouration : Due to most specimens being previously treated with NaOH, here we consider only the cuticular colouration, which is less influenced by the hydroxide, thus overall patterns are retained. The majority of Holopothrips species are uniformly brown, although the shade of brown is variable from very dark, almost black ( Figs 26 , 191 , 198 ) to light or yellowish brown ( Figs 107 , 226 ), with some specimens of H. varicolor sp. n. being almost yellow. Twelve species of Holopothrips have the abdomen strikingly bicoloured: four of them have the body mainly brown with only abdominal segments II–III yellow ( Fig. 222 ), or abdominal segments II–V in H. hilaris ; and the remaining eight have the body mainly yellow, with only the head, abdominal segment X, and sometimes segments VIII–IX brown ( Figs 32 , 51 , 95 ). The more frequent pattern of colouration for the legs is having all femora concolourous with the body, mid and hind tibiae concolourous as well but lighter near apex (from just the tip to apical third or half), fore tibiae and all tarsi yellow or clearly lighter than fore femora ( Figs 16 , 131 , 138 ). However, exceptions are not uncommon, such as the fore tibiae being brown in several dark-bodied species ( Figs 26 , 69 , 191 ), or all tibiae being almost white in H. claritibialis ( Fig. 55 ), or the brown species H. pennatus having all legs fully yellow ( Fig. 211 ). An uncommon variation is the presence of yellow hind femora but brown hind tibiae in H. hilaris and H. signatus ( Fig. 222 ), although in the latter species individuals have been reported with brown hind femora ( Hood 1914 ). Antenna also presents some variation: usually segments I–II are concolourous with head, III–VI lighter or bicoloured, due to being shaded on apical half, and VII–VIII shaded or brown ( Figs 16 , 188 ). Some species have the antenna yellow on segments III–VIII ( Figs 211 , 226 ), and some bicoloured species may have segment III brown basally ( Figs 210 , 221 ). The fore wings may be hyaline ( Figs 26 , 69 ) or shaded yellow or light brown ( Figs 91 , 63 , 138 ). The basal area, especially around the sub-basal setae, is shaded in several species ( Figs 45 , 191 ). The median dark line on fore wing is usually absent, or only weakly indicated. Head : Several characteristics are variable and helpful for species identification. Firstly, the ratio between head length and width, which ranges from head slightly wider right behind eyes than long in H. flavisetis sp. n. ( Fig. 88 ), and some individuals of H. inconspicuus sp. n. , H. mariae , H. singularis sp. n. and H. varicolor sp. n. ( Figs 109 , 242 , 277 ), to over 1.8 times as long as wide in H. oaxacensis and H. permagnus ( Hood 1938 ; Johansen 1986 ) ( Fig. 212 ). However, the majority of Holopothrips species lie in between these extremes, having heads between 1.1–1.4 times as long as wide. The head proportions can be influenced by pressure during the mounting process (which can be noticed by shorter distance between dorsal and ventral views, head crushed or looking wider posteriorly, and thorax’ lateral margins greatly curved due to pressure), so specimens that were not flattened by pressure should be used for the analysis of this character. Head sculpture is usually formed by weak transverse lines, but in H. ananasi it is markedly reticulate ( Fig. 22 ), and in H. singularis sp. n. the sculpture is irregularly reticulate ( Fig. 242 ). Few species bear minute tubercles in the angles of dorsolateral sculpture ( Figs 227 , 236 ), giving the area a punctuate appearance. Compound eyes are frequently large, bulbous, sometimes bean-shaped ( Figs 96 , 223 , 267 ), this being a characteristic commonly associated with Holopothrips . However, some species do not have eyes so enlarged, but somewhat reduced in comparison to the eyes of other Holopothrips species ( Figs 46 , 88 ). There is one pair of postocular setae in almost all Holopothrips species, although in H. fulvus and H. singularis sp. n. they seem to be reduced to the size of discal setae ( Fig. 79 ), or fully absent ( Fig. 242 ). The length of po can range from barely different from discal setae ( Figs 52 , 235 ) to longer than the dorsal length of the eye ( Figs 160 , 199 ); but is usually between these extremes, about as long as the dorsal width of an eye. A third major seta or even a secondary pair of large setae may be present inner to po in some specimens ( Fig. 139 ); it is possible that this extra po is actually one of the postocellar pairs. The tip of po setae is as variable as the pronotal setae, less commonly acute (e. g. H. porrosati , H. stannardi ) or blunt (e. g. H. atlanticus sp. n. , H. magnus sp. n. , H. orites ), with expanded or capitate tips being more frequent (e. g. H. claritibialis , H. maiae sp. n. , H. tenuis ). The maxillary stylets vary in position within the head, the most common combination being retracted until postocular setae and about one third of head width apart or less ( Figs 96 , 99 , 113 ). Few species have the maxillary stylets retracted to the posterior margin of eyes and closer to each other medially, almost touching in H. ananasi , H. cardosoi sp. n. or H. conducans ( Figs 22 , 46 , 61 ). Other species have the maxillary stylets less retracted into the head, sometimes barely leaving the mouth cone ( Fig. 109 ) or, in species with a longer head, reaching halfway to po base ( Figs 169 , 192 ). Stylets less retracted into the head tend to be more separated from each other, having a V shape ( Figs 132 , 227 ) in contrast to the usual parallel disposition ( Figs 66 , 242 ). Mouth cone can be somewhat rounded at tip, and in this case the labial palps tend to be reduced to what looks like a basal plate, barely projecting from the labium ( Figs 187 , 243 ). In contrast, there are several Holopothrips species with the mouth cone longer and pointed, sometimes extending beyond the posterior margin of fore coxae, with labial palps usually being longer and with visible segmentation ( Figs 173 , 278 ). Antenna : With eight segments in all Holopothrips species; the main antennal character used for species identification is the number of sense cones on segments III–IV. Three sense cones on each seems to be the most common pattern within the genus, but reductions in the number of sense cones occur in a variety of species ( Mound & Marullo 1996 ). Species such as H. carolinae , H. graminis , H. longisetus sp. n. bear only two sense cones on antennal segments III–IV. There are also species where the number of sense cones is variable, such as H. jaboticabae (one or two cones on III and two or three on IV), H. fulvus (usually three sense cones on both segments, but in some specimens one sense cone is absent) ( Lima et al. 2017 ), or H. mariae (usually with two sense cones on each segment, but some individuals have three sense cones on III) ( Mound & Marullo 1996 ). This variation seems to be present as well in H. flavisetis sp. n. , with the observed females bearing two sense cones on IV and the single available male bearing three sense cones. Prothorax : Pronotal sculpture is usually weak or absent medially, being present only near the posterior margins, and sometimes anterior margins. In H. reticulatus sp. n. the pronotum is fully reticulate, and in H. singularis sp. n. the sculpture is absent only in a small median portion of pronotum. All five pairs of major pronotal setae are usually present, although reductions in size are not uncommon. Several species have the am setae reduced ( Figs 99 , 177 , 227 ), not differing from discal setae, or with variable length among individuals of the same species ( Figs 160, 162 ). In some other species the aa setae are minute ( Figs 96 , 267 ), and in few of these the ml also arises closer to the anterior margin. The length of pronotal setae in general also varies greatly, with some species having these setae (except ep) very short ( Figs 169 , 273 ), and others having elongate setae, with ep and pa longer than 100 µm ( Figs 152 , 160 ). The epimera usually bear one pair of major setae, but a second minute seta is present close to the major pair. In some species this second pair is fully developed, thus the epimeral region bears two pairs of major setae ( Figs 61 , 169 , 192 ). The apex of pronotal setae is also variable, most frequently expanded or capitate ( Figs 22 , 259 ), sometimes blunt ( Figs 27 , 169 ), and some species may have some setae acute (e.g. H. stannardi ). Not all setae have the same type of apex, with smaller setae (usually am and/or aa) frequently having acute or blunt apex in contrast to the capitate tips of longer setae. Mesonotum : The mesonotal sculpture ranges from well-defined equiangular reticles ( Figs 100 , 229 ) to elongate or irregular reticles ( Figs 22 , 216 ) to mostly transverse lines ( Figs 193 , 207 ). While most Holopothrips species do not have internal markings within the mesonotal sculpture, several species bear them, sometimes weaker and restricted to a few reticles ( Fig. 127 ), in others well-defined and filling all reticles ( Figs 76 , 216 ). Sometimes the median sculpture converges towards the posteromedian suture of mesonotum, with the sculpture becoming elongate or almost striate. Metathorax : Similar to the mesonotum, the metanotum bears variable sculpture, especially on median and posterior areas. Laterally the sculpture tends to be formed by elongate reticles or striations, independent of the median pattern. The most common pattern medially seems to be longitudinally elongate reticles, sometimes weakly defined and without internal markings ( Figs 19 , 47 ), in others well-defined, with internal markings ( Figs 134 , 237 ) or without them ( Figs 190 , 281 ). A few species, such as H. hambletoni or H. punctatus sp. n. , have the metanotum covered by equiangular reticles, usually without internal markings or with faint ones ( Figs 100 , 233 ). In some species the metanotal sculpture is striate, either through the whole sculptured area ( Figs 67 , 200 , 208 ) or on anterior half, with elongate to equiangular reticulation covering the posterior half ( Figs 128 , 269 ). Although more uncommon, striate sculpture can also bear weaker lines in between the striae, which are also considered internal markings here ( Fig. 147 ). Anterior to the major median setae of the metanotum, all Holopothrips bear at least one or two shorter setae. While most species have one or two pairs of these setae, H. bicolor sp. n. usually bears more than five pairs of setae, frequently asymmetrically placed ( Fig. 38 ). This trait is not exclusive to the genus, being found in a variety of Phlaeothripidae species (called the “group c” of metanotal setae in Bhatti (1998) , which also mentions several genera unrelated to Holopothrips that bear these setae). Ventrally, most Holopothrips have well-defined metapleural sutures, although in H. carolinae , H. hilaris , H. tillandsiae and H. tupi they seem to be reduced, and in H. johanseni sp. n. , H. longisetus sp. n. , H. pictus and H. signatus no metapleural suture is observed ( Fig. 144 ). In at least H. inconspicuus sp. n. and H. singularis sp. n. the metapleural suture seems to be variable within the species, being present in some individuals but not visible in others. Abdomen : The presence of a third pair of WR on tergites II–VII is usually mentioned as one of the diagnostic features of the genus, being found in most species ( Figs 18 , 60 ). However, species such as H. inconspicuus sp. n. , H. jaboticabae ( Fig. 124 ), H. tillandsiae and H. varicolor sp. n. frequently lack this third WR in several tergites, and in the species H. flavisetis sp. n. and H. infestans sp. n. the third WR is mostly absent from all tergites. While usually smaller than the other two WR pairs, the third pair may be well-developed and sigmoid, or small and weakly curved, sometimes easily confused with lateral setae. Some other Phlaeothripidae genera (e.g. Euoplothrips Hood , Mesothrips Zimmerman , Pristothrips Hood ) may have three or more pairs of wing-retaining setae, usually multiple pairs on abdominal tergites II–IV, but these seem to be related to the large bodies of these species. The shape of the pelta is highly variable: in some species it is sharply triangular ( Fig. 179 ), in others triangular but with irregular ( Figs 71 , 194 ) or curved ( Figs 164 , 200 , 261 ) margins, and in a few species with a median constriction ( Figs 117 , 123 ). Holopothrips ananasi and H. kaminskii sp. n. are unique in having the pelta with large lateral wings basally, that in the latter species is associated with a constriction, giving this species a bell-shaped pelta ( Figs 23 , 149 ). Sculpture is always present, usually formed by reticles covering the whole pelta ( Figs 117 , 280 ), but sometimes sculpture is weaker or absent near the posterior area ( Figs 240 , 244 ), lateral margins ( Figs 128 , 172 ) or medially ( Fig. 164 ). The reticulation may be almost equiangular ( Figs 36 , 252 ) or elongate ( Figs 200 , 208 ) medially, and internal markings may be present ( Figs 261 , 275 ) or absent. Pore plates : In males of Holopothrips these are frequently present on more than one sternite, usually VII–VIII ( Figs 59 , 129 ), sometimes VI–VIII ( Figs 35 , 101 ) or V–VIII ( Fig. 246 ), with H. brevicapitatum sp. n. having plates in sternites IV–VIII ( Fig. 42 ). On sternite VIII the usual pattern is the presence of three pore plates, two anteroangular plates and a transverse band posterior to the discal setae, usually reaching the lateral margin of the sternite ( Figs 129 , 181 ). Median interruptions in the posterior plate are not uncommon, and in some species such an interruption may be large enough to separate this plate into two lateral bands ( Fig. 82 ). In some species, the two anteroangular plates may be absent ( Figs 48 , 203 ), and the remaining posterior plate may be reduced to a small median band ( Figs 21 , 65 ). In a few species the posterior plate of sternite VIII might extend laterally onto the tergite, from barely reaching the spiracle to almost encircling the segment ( Fig. 130 ). Several Holopothrips species also have the pore plates with a clear reticulate pattern ( Figs 68 , 181 ), contrasting to the usual punctate appearance of pore plates in other Phlaeothripinae species. Intraspecific variation of pore plates has been observed in some species, such as H. claritibialis ( Cavalleri & Kaminski 2007 ) . These authors reported the presence of median interruptions in the posterior plate and differences in the area occupied by the pore plates among specimens, as well as the presence of connections between the anteroangular plates and the posterior plate in few individuals; these connections were also observed in other species such as H. maiae and H. nigrisetis ( Fig. 196 ). Few Holopothrips species are known to have males lacking pore plates. In this work, we observed the absence of pore plates in H. graminis , H. inconspicuus sp. n. , H. kaminskii sp. n. , H. longisetus sp. n. , H. molzi and H. tillandsiae . Mound & Marullo (1996) also mention in their key that males of H. seini and H. urinator do not have pore plates. Spermatheca : This is visible in all observed species of Holopothrips even after maceration, possibly being more sclerotized than in other Thysanoptera species. It seems to be a useful diagnostic character for the group, as the spermatheca is rarely seen in other phlaeothripids. Some species have the spermatheca swollen medially ( Figs 24 , 94 ), while in others it is curled and not enlarged ( Figs 30 , 49 , 265 ). When enlarged, these structures vary from only slightly enlarged medially ( Figs 81 , 206 ) to greatly swollen or almost round medially ( Figs 136 , 283 ). When not enlarged medially, the spermatheca may vary among species from very thin ( Figs 98 , 268 ) to greatly thickened ( Fig. 165 ). While usually small and restricted to abdominal segment IX, in H. tillandsiae the spermatheca is very elongate, with some curls reaching abdominal segment VI ( Zamora et al. 2015 ). We did not observe any intraspecific variation in shape and size of this structure, even when comparing females with and without eggs in their abdomen. Fore legs : Unarmed in all species, but the fore tarsal hamus is robust or greatly enlarged in three species: H. brevicapitatum sp. n. , H. longihamus sp. n. and H. longisetus sp. n. ( Figs 153 , 161 ). The fore femora in some species may be robust, but never greatly swollen ( Figs 40 , 152 , 276–277 ). Fore wings : Always macropterous and with margins parallel. There is variation in the shape of the tip of the sub-basal setae, which seems to agree with the shape of tip of other major body setae. With the exception of H. carolinae , all species bear duplicated cilia on fore wings, but the number is highly variable among species (from 4 or 5 cilia in H. mariae to 16–27 in H. nigrum sp. n. ), within species, and between the right and left fore wings of the same individual ( Cavalleri & Kaminski 2007 ).