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Home , Centaurea, Centaurea solstitialis, Centaurea sulphurea, Cirsium cymosum

A lace bug as biological control agent of yellow starthistle, solstitialis L. (): an unusual choice

A. Paolini,1 C. Tronci,1 F. Lecce,1 R. Hayat,2 F. Di Cristina,1 M. Cristofaro3 and L. Smith4

Summary The lace bug Tingis grisea Germ. (Hemiptera: Tingidae) is a univoltine sap-feeder associated with the Centaurea L. and distributed throughout Central and Southern Europe and the . In 2002, one Turkish population of T. grisea was selected as a potential biological control agent for yellow starthistle, L., (Asteraceae: Cardueae), a of primary concern in the USA. Field observations showed that significant damage was caused to the host especially when many individuals were feeding on the same plant. Life-cycle and biology observations were made to assess the duration of the five nymphal instars of T. grisea under laboratory conditions, as well as female fecundity and longevity. Starvation and oviposition no-choice tests were carried out in order to determine the host specificity of the . Results showed a clear oligophagous behaviour closely restricted to the genus Centaurea. In addition, among the three Centaurea spp. on which full larval development was ascertained (C. solstitialis, , Centaurea ), yellow starthistle was clearly most suitable regarding number of eggs laid and number of adults obtained.

Keywords: YST, host range, Tingis grisea.

Introduction var. solstitialis Otth., has been released (Woods, 2004; Fisher et al., 2006), and two beetles are being evaluated Yellow starthistle, Centaurea solstitialis L., (Aster- (Cristofaro et al., 2004; Smith, 2004; Smith, 2007); all aceae: Cardueae) is an important invasive alien weed of these attack immature . However, it would also of in the western and is the be useful to have an agent that stresses the plant later in target of a USDA classical biological control program the growing season, during the critical period when it (Turner et al., 1995; Sheley et al., 1999; Smith, 2004; is flowering and producing (Smith, 2004). During Di Tomaso et al., 2006). Six insect agents that attack foreign exploration for new biological control agents in C. solstitialis flowerheads have already been introduced eastern in 2002, we discovered a large popula- (Cristofaro et al., 2002; Pitcairn et al., 2004), but they do tion of the lace bug Tingis grisea Germ. 1835 (Hemi- not appear to be reducing the weed population sufficient- ptera: Tingidae) feeding on mature C. solstitialis rosettes ly (Pitcairn et al., 2000, 2006). Therefore, it is desirable and on bolting plants. to find new agents that attack other organs of the plant In the literature, this lace bug has been reported or earlier phenological stages. A , Puccinia jaceae from 11 of Centaurea, including C. solstitia- lis, as well as from vulgaris L. (Stusak, 1959), a very closely related plant species (Susanna et al., 1995). Its geographical distribution is very wide: it 1 Biotechnology and Biological Control Agency, Via del Bosco 10, 00060 occurs from central across southern Europe to Sacrofano, Rome, . 2 Atatürk University, Faculty of , Plant Protection Depart- southern Russia; generally overlapping the distribution ment, 25240 TR Erzurum, Turkey. of C. solstitialis and some close relatives (Komarov, 3 ENEA C.R. Casaccia BIOTEC, Via Anguillarese 301, 00123 S. Maria 1934; Klokov et al., 1963; Wagenitz, 1975; Dostál, di Galeria, Rome, Italy. 1976). Little is known about its biology (Stusak, 1959; 4 USDA-ARS, 800 Buchanan Street, Albany, CA 94710, USA. Corresponding author: A. Paolini . Péricart, 1983). T. grisea is reported as univoltine and © CAB International 2008 overwinters as adult. Oviposition begins in May, and

189 XII International Symposium on Biological Control of eggs are inserted into the young tissue of stems and ax- ings and richness of trichomes), it was impossible to ils. Eggs are very small; the operculum measures 0.16 ´ count eggs. Thus, we indirectly evaluated oviposition 0.05 mm (Stusak, 1957). In Ukraine, nymphs appear success by retrieving emerged nymphs from stems ex- at the beginning of June and adults at the beginning of posed to . In 2006, insects were tested on leaves July. Five nymphal instars have been described. instead of stems. In fact, preliminary trials carried out This paper reports results of studies on the life cy- at the beginning of the season showed that T. grisea is cle, rearing and host-plant specificity of this insect to able to lay eggs both on leaves and on stems. In this determine whether it warrants further evaluation as a way, we were able to see eggs by observing leaves un- candidate for biological control of yellow starthistle. der the stereo microscope with backlighting. Leaves with eggs were stored in a plastic box on tissue paper until nymph emergence. Each pair was kept on yellow Methods and materials starthistle before and after being tested on any other Collection of insects plant species in order to give the insects the possibility to feed on the host plant and to be sure that females Insects emerging from winter diapause were col­ were actually ovipositing. Replicates on test plants lected in late March of 2004, 2005 and 2006 in the were considered invalid if the continuity of a female’s vicinity of Horasan (Erzurum Region, 1600 m ASL), oviposition ability could not be demonstrated on C. sol- Eastern Turkey. In the laboratory, lace bugs were kept stitialis after a replicate with zero eggs on any non-host in a 3-l glass beaker at low temperature (8°C) and plant. Two to 11 specimens for each plant species were 12:12 h L/D photoperiod. Insects were allowed to feed tested in 2004 and 2006; the plants tested are listed in on freshly cut leaves of C. solstitialis (US biotype) held Table 1. in water vials; crumpled tissue paper was also provided as shelter for insects to rest. Larval transfer experiment Laboratory rearing Nymphs of T. grisea (two to six per replicate) were transferred to intact leaves of potted C. solstitialis and Insect rearing was carried out on natural substrate, other test-plant species, confined in transparent plastic using potted plants of C. solstitialis (US biotype) at cylinders at 23°C to 26°C and 16:8 h L/D. The first 23°C to 26°C and 16:8 h L/D. Single pairs of T. gri- observation occurred after 7 days in order to assess sea were confined to a portion of yellow starthistle nymphal development and mortality. Afterwards, ob- stem anchored in a foam disk on the bottom of a 17 ´ servations were carried out every 3 to 4 days until all the 5 cm transparent plastic cylinder, capped with fine ny- nymphs either reached the adulthood or died. For each lon mesh. A hole in the side, closed by a foam plug, plant species, we tested an average of five specimens. was used for insect manipulation. After 7 days, insects Plants tested from 2004 to 2006 are listed in Table 2. were removed and transferred to another stem under the same conditions. Beginning 10 days after insect exposure, stems were cut off and daily examined un- Results and discussion der a stereo microscope to search for neonate nymphs. Life cycle The same procedure was repeated several times for each pair of insects. Emerged nymphs were used for Life-cycle observations, carried out during labora- host-range, larval transfer experiments and life-cycle tory rearing and oviposition and larval transfer trials, observations. show that under laboratory conditions (23°C to 26°C, 16:8 h L/D), first-instar nymphs emerged 10 to 12 days Host specificity after oviposition. The duration of the first and second larval stages was approximately 3 to 4 days, while the The host specificity of the insect was assessed by development of each stage, from third to fifth instars, means of no-choice tests on plant species related to took 7 to 8 days. Total development was approximately yellow starthistle, including US native and US com- 31 days (Figure 1). mercial . No-choice oviposition experiment No-choice oviposition experiment Results of no-choice oviposition tests, performed in In 2004, stems of C. solstitialis (US biotype) and 2004 and in 2006, clearly showed that T. grisea ovipos- other test plants were exposed to a pair of insects in its most on C. solstitialis and, with limited success, on transparent cylinders at 23°C to 26°C and 16:8 h L/D. closely-related species (Table 1), including Centaurea After 3 to 4 days, insects were removed and stems ob- stoebe, , , Centau- served under the stereo microscope in order to count rea sulphurea and Acroptilon repens. In 2004, oviposi- eggs. Because of the extremely small size of egg oper- tion occurred on only three of the eight plant species cula and the complexity of stem features (tissue fold- tested. The number of larvae that emerged per replicate

190 Table 1. Summary of no-choice oviposition tests carried out in 2004 and 2006. 2004 No-choice oviposition 2006 No-choice oviposition Number of Number of Valid Non-valid Number of Number of Number of Number of % emerged Valid Non-valid Number of Number of plants tested emerged replicates replicates larvae/valid plants tested eggs laid emerged larvae replicates replicates eggs/valid larvae/valid larvae replicates larvae replicates replicates Subtribe: Centaureinae Acroptilon repens 3 5 0 0 3 0 1.7 0 tinctorius - 5 0 3 3 0 6 0 0 0 2 5 0 0 Linoleic Carthamus tinctorius - 5 0 3 3 0 5 0 0 0 2 3 0 0 Oleic Crupina vulgaris 3 0 2 1 0 Genus: Centaurea Centaurea cyanus 3 4 3 1 1.3 5 4 1 25 2 4 2 0.5 Centaurea diffusa 3 6 1 17 3 0 2 0.3 4 5 2 2 2.5 3 0 0 0 2 1 0 0 Centaurea solstitialis 16 22 25 19 0.9 19 266 106 40 59 19 4.5 1.8 Centaurea sulphurea 2 3 0 0 2 0 1.5 0 Subtribe: Carduinae Carduus 2 0 0 0 0 2 0 0 pycnocephalus brevistylum 2 0 0 0 0 2 0 0 Cirsium hydrophilum 2 0 0 0 0 2 0 0 Cirsium loncholepis 3 0 0 0 0 3 0 0 Cirsium occidentale 2 0 0 0 0 2 0 0 Cynara scolymus 4 0 2 2 0 2 0 0 0 0 4 0 0 Tribe: Heliantheae Helianthus annuus 3 0 0 0 0 3 0 0 XII International Symposium on Biological Control of Weeds

59 64 28 20 55 10 20 47 20 10 10 26 26 10 10 36 27 transferred larvae Total

4 2 2 4 8 3 1 2 6 6 1 2 5 5 12 12 12 tested plants Total 0 3 0 0 0 0 0 29 73 25 10 adult % developed

29 31 10 28 10 15 20 16 16 10 17 L3 or L4 Number of larvae transferred 2 3 4 4 1 4 7 6 1 7 2 a Number of plants tested 0 0 0 0 0 0 0 0 0 0 0 0 0 0 41 63 adult % developed fourth-instar nymphs.

L4 Stage of larvae transferred 0 0 0 0 0 0 0 6 0 0 81 10 20 56 30 30 L3 % developed

L1 or L2 third-instar nymphs, 30 33 18 20 27 10 10 32 10 10 10 10 10 10 26 10 L3 Number of larvae transferred

5 6 3 2 5 2 2 6 1 2 2 2 1 2 4 1 Number of plants tested second-instar nymphs, L2

Summary of the larval transfer results conducted during 2004 to 2006. First-instar nymphs, Carthamus tinctorius - Linoleic Centaurea Helianthus annuus Carduus pycnocephalus Carduus Cirsium brevistylum Carthamus tinctorius - Oleic Crupina vulgaris cyanus Centaurea diffusa Centaurea stoebe Centaurea melitensis Centaurea rothrockii Centaurea solstitialis-CA Centaurea Cirsium cymosum Cirsium hydrophilum Cirsium loncholepis Cirsium occidentale Cirsium vinaceum Cynara scolymus Acroptilon repens Acroptilon Centaurea sulphurea Centaurea L1 Subtribe: Centaureinae Genus: Centaurea Subtribe: Carduinae Heliantheae Tribe:

Table 2. Table a

192 A lace bug as biological control agent of yellow starthistle, Centaurea solstitialis L. (Asteraceae)

Figure 1. Diagram of estimated development time of immature stages of Tingis grisea under labora- tory conditions (23 + 3°C, 16:8 h L/D photoperiod). was 0.9 on C. solstitialis, 1.3 on C. cyanus and 2.5 on Conclusions C. stoebe. The total number of nymphs emerged was considerably higher on yellow starthistle, although it Preliminary host-specificity results, obtained from was very low compared to the number of replicates car- 2004 to 2006, showed clear oligophagy by T. grisea. ried out (Table 1). Lack of knowledge about develop- Among the species on which oviposition occurred (C. ment times of the insect in this preliminary phase, in cyanus, C. stoebe, C. diffusa, C. sulphurea and A. re- addition to a relatively low survival rate of the eggs on pens), the target weed C. solstitialis was clearly pre- cut stems, was probably responsible for this low number ferred in terms of number of eggs laid and number of of nymphs recorded. nymphs emerged. In addition, only a few nymphs that In 2006, females laid nearly 94% of their eggs on were transferred to non-target plants completed devel- yellow starthistle, and 40% of them produced nymphs. opment on species closely related to yellow starthistle The relatively low emergence rate can be attributed (C. cyanus and C. sulphurea). 3rd instar nymphs could to low egg survival on cut leaves due to rapid wither- sometimes develop on critical nontarget plants, such as ing and occurrence of mould. Although we found eggs C. tinctorius and C. scolymus, but transfer of 3rd and on C. cyanus, C. diffusa, C. sulphurea and A. repens, 4th instar nymphs represents an extreme situation that nymphs emerged only from eggs laid on C. cyanus and is not likely to occur in the field because the nymphs C. diffusa. In both C. sulphurea and A. repens, leaves are not highly mobile. Failure of young larvae to de- with eggs became mouldy several days after oviposi- velop on C. americana is very promising because this tion, thus further experiments are needed to improve is the closest native North American relative to the tar- the measure of nymphal emergence on these plants. get weed. Further feeding and oviposition trials under no- Larval transfer experiment choice and choice conditions are required to better de- fine the host range of this insect and understand if it In larval development no-choice tests carried out represents a good candidate for the biological control from 2004 to 2006, nymphal survivorship was greatest of C. solstitialis. Moreover, laboratory tests and open- on yellow starthistle (Table 2): 63% of first and sec- field trials are needed to evaluate its impact on the tar- ond instar nymphs and 73% of third and fourth instar get species. nymphs reached the adult stage on C. solstitialis, while a smaller percentage was able to complete the devel- opment on a small number of closely related species Acknowledgements (C. cyanus and C. sulphurea). In general, development and survival was greater for old nymphs than for young We are grateful to Levent Gültekin and Göksel Tozlu, ones, on both the target and nontarget plants. We ob- Atatürk University (Erzurum, Turkey), for their sup- served development of one adult from 3rd instar on an port in field collections. oleic variety of Carthamus tinctorius and one on Cy- nara scolymus, but none of the younger (1st and 2nd References instar nymphs) became adults. This insect is not a of either of these crops, which suggests that transfer of Cristofaro, M., Hayat, R., Gultekin, L., Tozlu, G., Zengin, 1st and 2nd instars is more valid than transfer of 3rd H., Tronci, C., Lecce, F., Sahin, F. and Smith, L. (2002) and 4th instars. Preliminary screening of new natural enemies of yellow

193 XII International Symposium on Biological Control of Weeds

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