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Revista de la Sociedad Entomológica Argentina

versión impresa ISSN 0373-5680

Rev. Soc. Entomol. Argent. vol.72 no.1-2 Mendoza jun. 2013

 

TRABAJOS CIENTÍFICOS

A new Neotropical species of Liothrips (Thysanoptera: Phlaeothripidae) associated with Ludwigia (Myrtales:Onagraceae)

Una especie nueva Neotropical de Liothrips (Thysanoptera: Phlaeothripidae) asociada con Ludwigia (Myrtales: Onagraceae)

 

Zamar1, María I., María C. Hernández2, Gerardo A. Soto-Rodríguez3, Axel P. Retana-Salazar3

1Instituto de Biología de la Altura, Universidad Nacional de Jujuy. Avenida Bolivia 1661 (4600) San Salvador de Jujuy, Argentina; mizamar@inbial.unju.edu.ar
2Fundación para el Estudio de Especies Invasivas, (FuEDEI), General Simón Bolívar 1559 (B1686), Hurlingham, Buenos Aires, Argentina: e-mail: crishernandez@fuedei.org
3Programa Universitario de Especial Interés Institucional en Biología Aplicada (PUA), Centro de Investigación en Estructuras Microscópicas (CIEMIC), Ciudad de la Investigación, Universidad de Costa Rica 2060. cultivosyasesorias@yahoo.com; axel.retana@ucr.ac.cr/ apretana@gmail.com

Recibido: 10-X-2012;
Aceptado: 22-IV-2013

 


ABSTRACT. Liothrips ludwigi (Thysanoptera: Phlaeothripidae) is described and a key to differentiate it from the other four species present in Argentina is provided. This species can be distinguished by the following characters: major setae on head and pronotum slender and brown yellowish; anteromarginal setae short (14µ-21µ), and metanotum reticulated with hexagonal cells. Liothrips ludwigi feeds and reproduces on Ludwigia grandiflora (Michx.) Greuter & Burdet and L. grandiflora ssp. hexapetala (Hook. & Arn.) G.L. Nesom & Kartesz (Myrtales: Onagraceae). This is the first record of the association between Liothrips and this family of plants.

KEY WORDS. Morphology; Biological characteristics; Damage; Biological control; Thrips.

RESUMEN.  Se describe Liothrips ludwigi (Thysanoptera: Phlaeothripidae) y se presenta una clave para diferenciarla de las otras cuatro especies citadas para la Argentina. Esta especie se distingue por los siguientes estados de caracteres: setas mayores de la cabeza y del pronoto, delgadas y de color castaño amarillento, setas anteromarginales cortas (14µ-21µ) y metanoto reticulado con celdas hexagonales. Liothrips ludwigi se alimenta y reproduce sobre Ludwigia grandiflora (Michx. Greuter & Burdet), y sobre L. grandiflora ssp. hexapetala (Hook. & Arn.) G. L. Nesom & Kartesz (Myrtales: Onagraceae); siendo éste el primer registro de asociación de Liothrips con esta familia de plantas.

PALABRAS CLAVE: Morfología; Características biológicas; Daños; Control biológico; Trips.


 

INTRODUCTION

Liothrips (Uzel) is one of the three most numerous genera of Thysanoptera with 260 species (Mound, 2005) which are difficult to differentiate; even the genus diagnosis is still unsatisfactory. A large proportion of the species were described from a single sample or specimen, which impedes the recording of inter- and intra-population variations (Mound & Marullo, 1996; Mound & Pereyra, 2008).
The genus Liothrips utilizes a wide range of host plants distributed in 28 families; however, 93% of its known species were recorded in only one host, indicating an eventual monophagy of this genus (Cock, 1982). Due to the Liothrips taxonomic complexity, more in-depth studies should be conducted (Del Claro & Mound, 1996; Mound & Pereyra, 2008).
Four Liothrips species are recorded for Argentina: Liothrips atricolor De Santis (1950), Liothrips tandiliensis (Liebermann & Gemigniani, 1931), Liothrips vernoniae Moulton (1933), Liothrips tractabilis Mound & Pereyra (2008). The first three species are only known from the type specimen, and the first two have no information on the host plant.
The new Liothrips species described in this paper was collected while looking for biological control agents for Ludwigia grandiflora ssp. hexapetala (Onagraceae). This South American aquatic weed has spread in freshwater bodies across the United States and Europe, causing severe ecological and economic damages (Okada et al., 2009; Haury et al., 2011; Nehring & Kolthoff, 2011). Ludwigia grandiflora and other six to eight species grouped in Oligospermum section are considered a polyploid complex with hybridization among some of the species (Zardini et al., 1990; Nesom & Kartesz, 2000; Wagner et al., 2007).
In this contribution a new species of Liothrips is described and a key to the Argentinean species is presented. In addition, biological information, such as development time, feeding behavior, and reproduction sites, is reported.

MATERIAL AND METHODS

The Liothrips specimens were collected in Argentina on Ludwigia grandiflora, and L. g. ssp. hexapetala which grows in shallow water bodies with slow or null stream. The collecting sites were: (1) Corrientes Province, Rd. 12, km 1219 near Itá Ibaté (27º 35' 58.3''S - 57º 02' 02.1''W); (2) Santa Fe Province, Rd.1, North of El Gusano (29º 35' 48.7''S -59º 46' 41.4''W); (3) Rd. 11, 7 km S Santa Fe city (31º 40' 31.1''S - 60º 44' 24.1''W); and (4) Buenos Aires Province, Rd. 9, Otamendi (34º 12' 46.7''S - 58º 53' 26.7''W). Stems of Ludwigia species were cut in the field, transported to the laboratory in plastic bags, and analyzed under stereoscopic microscope; Liothrips specimens obtained were cultured on Ludwigia g. ssp. hexapetala plants. A subsample of individuals was preserved in 70% ethanol for taxonomic purposes.
Morphological studies were carried out on permanent slide-mounted specimens following Mound & Kibby (1998); a genus-level key of Phlaeothripinae (Mound & Marullo, 1996) and two species-level keys (Karny, 1912; Mound & Pereyra, 2008) were used. In addition, specimens were compared with described Neotropical species of Liothrips (Moulton, 1933; Hood, 1938; Johansen, 1974, 1979).
The type specimens and series were housed as follows: Holotype, female and paratype series, at La Plata Museum (MLP); paratype series at the Instituto de Biología de la Altura, Universidad Nacional de Jujuy (INBIAL-UNJu) and at the Fundación para el Estudio de Especies Invasivas (FuEDEI, formerly USDA-ARS-SABCL) in Argentina. Also, paratype series were deposited at the Colección Institucional de Thysanoptera (CIT), Centro de Investigación en Estructuras Microscópicas (CIEMIC), Universidad de Costa Rica, Costa Rica.
A culture of Liothrips sp. nov. was established on L. g. ssp. hexapetala plants in a pot (30x40cm) inside an escape-proof nylon cage (60x60x60cm) located outdoors. During winter, the cage was covered with transparent plastic to avoid freezing   temperatures.   Periodically, new fresh stems were added to the pot to replace those damaged by feeding. The biological observations were obtained both from stems collected in the field and from specimens cultured in rearing chambers (25º± 1ºC; 12h light: 12h dark).
The life history of Liothrips sp. nov. was studied monitoring the development of eggs laid on apical stems of L. g. spp hexapetala held in escape-proof plastic containers (15x25 cm) with wet tissue paper in the bottom to provide moisture. The development was recorded daily and stems were changed when necessary.

RESULTS

Liothrips ludwigi sp. nov. (Figs. 1-11)


Figs. 1-2. Liothrips ludwigi sp. nov. 1, female macroptera, holotype; 2, male macroptera. (Scale bar: 1 mm).


Figs. 3-9. Liothrips ludwigi'sp. nov. holotype. 3, head; 4, antenna; 5, pronotum; 6, prothoracic sternum showing ferna large; 7, metanotum; 8, pelta; 9, abdominal tergites II-III. (Scale bar = 50)am).


Figs. 10-11. Liothrips ludwigi sp. nov., right wings. 10, forewing; 11, hind wing. (Scale bar= 0.5 mm).

Diagnosis: Female macropterous; blackish brown with red hypodermal pigment, the living individuals have tube reddish; antennal segments blackish brown except segment III brownish yellow, pale brown distally; setae brown yellowish; fore wings slightly shaded around margins and in a medial longitudinal line; clavus and sub-basal area brown. Dorsal setae are acute and some weakly capitates. Antennal segment III large, 2.4 times the maximum width. Postocular setae acute as long as eye length. Anteromarginal setae small. Basantra not developed, ferna present. Metanotum reticulated with hexagonal cells; bell-shaped reticulated pelta. Fore wings with 10-11 duplicated cilia and 3 weakly capitated basal setae. Anterior tarsi with hammus. Setae S1, S2 and S3 from tergite IX shorter than tube length. Male macropterous with a well-developed glandular area in the sternite VIII, but it does not reach the posteromarginal setae base.

Description. Female macroptera (Fig. 1). Body blackish brown; the living adults have red hypodermal pigment which combined with the blackish cuticle results in dark abdominal segments with a red band in the posterior edge; the same red bands are observed at the end of the head, the prothorax and the metathorax; in addition, in weakly sclerotized individuals the tube is reddish; brown yellowish setae; middle part of the fore tibiae and tarsi brown yellowish; lateral margin of fore tibia dark brown; antennal segments dark brown except segment III brownish yellow and pale brown distally; fore wings slightly shaded around margins and in a medial longitudinal line (Fig. 10); clavus and sub-basal zone brown; hind wings hyaline (Figs.10, 11). Dorsal setae acute, some slightly capitate. Head with cheeks slightly bend to the base; anterior ocellus located on a projection between the antennal bases; postocular setae acute and with the same length as eyes (Fig. 3). Maxillary stylets retracted reaching the postocular setae base, 0.3 of head width apart. Antenna with segment III elongated, pedicellate, approximately same length as segment IV, and with one external sensorium (Fig. 4); segment IV with three sensoria, two external and one internal. Pronotum wider than long (Fig. 5), with median carina, with five pairs of acute setae, small anteromarginal setae, posteroangular setae almost as long as 0.7 times the pronotum; basantra not developed (Fig. 6), ferna present; mesopraesternum undivided, metathoracic esternopleural suture short. Fore legs with hammus well developed; forewing with parallel sides and 10-11 duplicated cilia; three basal setae weakly capitate (Figs. 10, 11). Metanotum reticulate with hexagonal cells (Fig. 7); median setae acute. Pelta bell shaped, reticulated (Fig. 8). Tergite II-VII with two pairs of sigmoid setae, the second pair longer than the other (Fig. 9); tergal lateral setae sharp; tergite IX with S1, S2 and S3 acute; anal setae approximately same length of tube.
Measurements of the holotype female in microns (slide-mounted): Body length: 2940. Head, length: 294, width: 231. Mouth cone long: 105. Postocular setae: 91-105. Antennal segments, length (width), I: 42(49); II: 63(42); III: 84(35); IV: 91(42); V: 84(35); VI: 77(35); VII: 84(28); VIII: 49(14). Pronotum, length: 210; width: 406; anteromarginal setae: 14-21; anteroangular setae: 49; midlateral setae: 98-105; posteroangular setae: 140; epimeral setae: 161; metanotal media setae: 56. Forewings, length: 1093.7; sub-basal setae: 84-105-105. Tergite IX, S1: 252; S2: 126; S3: 196. Tube length: 280; basal width: 91; apical width: 56; anal setae: 259.
Male macroptera (Fig. 2). Similar to female but smaller and slenderer; fore tarsi without teeth; glandular area well developed in the mid sternite VIII, not reaching the base of the posteromarginal setae; setae in tergite IX acute.
Measurements of male paratype (in microns): Body length: 2587.5; head: length: 280; width: 203. Postocular setae: 70-91. Antennal segments, length (width): I: 36.4 (42), II: 56(35), III: 84(35), IV: 77(35), V: 70(35), VI: 63(35). VII: 77(28), VIII: 49(14.7).
Pronotum, length: 175; width: 322; Setae-anteromarginal: 7; anteroangular: 14-42; midlateral: 91; posteroangular: 140; epimeral: 126; metanotal: 49. Forewing, length: 968; sub-basal setae: 63-84-91. Tergite IX, S1: 224, S2: 77, S3: 238. Tube length: 252. Anal setae: 210.

Type material. Holotype female: ARGENTINA. Santa Fe: Rd. 1, N of El Gusano (29º35'48.7''S - 59º46'41.4''W), 11-III-2009, Cabrera col. (MLP). Paratypes: same data as holotype: 2 females, 1 male (MLP); 1 female, 1 male (FuEDEI); 1 female, 1 male (INBIAL-UNJU). Buenos Aires: Otamendi (34º12'46.7''S-58º53'26.7''W), august 2011, Hernández col., 1 female, (MLP); 2 females (FuEDEI); 3 females, 1 male (INBIAL-UNJu), 2 females, 2 males (CIT CIEMIC). Corrientes: Rd. 12, km 1219 near Itá Ibaté (27º35'58.3''S, 57º02'02.1'' W), 16.I.2008, Sacco and Sosa col., 1 female, 1 male (FuEDEI).

Key to Liothrips species from Argentina (Modified from Mound & Pereyra, 2008)

1.- Forewing margins weakly brown shaded (Fig.10) ......................... .....  ...............2
- Forewing margins hyaline .......  ...... ...  3

2.- Major setae on head and pronotum exceptionally stout and black; anteromarginal setae long (95µ); metanotum reticulated with elongated cells particularly in the posterior half ................... ......  ...... L. tandiliensis
- Major setae on head and pronotum slender and brown yellowish; anteromarginal setae  short  (14µ-21µ)  (Fig.5); metanotum
reticulated    with  hexagonal cells (Fig. 7)......... ..............  ....... L. ludwigi sp. nov.

3.- Antennal segments IV-V brown; segment III short, less than 3.0 times as long as maximum width................... L. tractabilis
- Antennal segments IV-V extensively or partially yellow; segment III slender, 3.0 times as long as maximum width or more than 3.0 times as long as maximum width... ...................................................4

4.-Postocular setae short, less than 0.35 times as long as head; metanotum reticulatestriate, with lines of sculpture closely parallel medially; tergite IX setae S1, S2 and S3 all with apices ........................... L. atricolor
- Postocular setae long, more than 0.4 times as long as head; metanotum reticulate, reticles longitudinally elongate medially; tergite IX setae S1, S2 and S3 all with apices pointed ................. ....  ........ L. vernoniae

Comments
Considering the general coloration of the wings of the Liothrips species found in Argentina, the new species is similar to L. tandiliensis; both have forewings weakly shaded around margins, but L. ludwigi has shorter antennal segments III and IV, and shorter postocular setae. The new species differs from L. atricolor, L. vernoniae and L. tractabilis which have hyaline wing margins; it can be distinguished from L. tandiliensis and L. tractabilis for having very short anteromarginal setae (14µ-21µ) while the others have long anteromarginal setae (90µ and 50µ respectively).
Liothrips ludwigi differs from the Neotropical species with shaded margin wings, Liothrips barronis Hood (1936), Liothrips vigilax Hood (1938) and Liothrips bispinosus Hood (1938), in the length of the anteromarginal setae; the three species have setae with 67µ, 40µ y 139-148µ respectively against the 14-21µ of L. ludwigi.

Biological characteristics: Currently, Liothrips ludwigi sp. nov. is being evaluated in Argentina as a biocontrol candidate of Ludwigia grandiflora ssp. hexapetala. It was observed feeding and breeding on the apical buds of L. grandiflora and L. g. ssp. hexapetala throughout the year (Figs. 12, 13). Adults and larvae share the same feeding-refuge sites in young leaves and they move to a new one when the leaves deteriorate. The females lay the eggs in the same leaves where they feed, preferably in the abaxial side and along the main veins. Eggs are cylindrical, with round equivalent poles, brown-whitish. Larvae I and 11  are red with dark brown heads, and dark brown antennal segments, pronotal plaques, legs, plaques in abdominal segment VIII, segment IX and X. The quiescent instars are completely red under a translucent cuticle; antennae, pterotecae and podotecae whitish. The development time from egg to adult was 35 days (egg: 7 (±1.1); larva I: 8 (±2); larva II: 12 (±3.1); prepupa: 3 (±1.4); pupa: 5 (±1.7).


Figs. 12-13. Liothrips ludwigi sp. nov. 12, adults overwintering hidden in young leaves; 13, group of adults (ad) and larvae (l).

In the quiescent instars they are hidden in dry leaves and have reduced mobility. They overwintered as adults sheltered in groups in the apical buds (until 12-15 individuals).

Damage: the thrips feed on the cell content in the epidermal and mesophyll tissues (Walling, 2000; Kindt et al., 2003); they form a canal with mandibles and maxillary stylets and suck the cell content. The plant reacts with a physiological process of defense (Walling, 2000) which, depending on the number of thrips, produces an energetic unbalance in the host. Ludwigia plants show the typical round spots in the feeding sites, curly or deformed leaves, dried apical buds and, if the attack persists, a general deterioration.

ACKNOWLEDGMENTS

We want to express our gratitude to Prof. J. Bhatti for his advice. To Dr. A. Cavallieri (Departamento de Zoología, Universidade Federal do Rio Grande do Sul) for his comments on the early manuscript. Thanks to Prof. Alexander Rodríguez-Arrieta and Dr. Roberto Johansen Naime for their help in the specimens comparison in the collection of IBUNAM in Mexico. Thanks to Guillermo Cabrera, G. Elsesser, E. Cuello, Julia and Ana Faltlhauser, and Juan Briano (FuEDEI) for the field collections, help with the rearings and manuscript readings.

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