Plant Protection Quarterly Vol.15(1) 2000 21 belonging to eight orders were found feeding on the plant (Figure 2, Table 2). The insect fauna associated with horehound The insects included 12 polyphagous spe- (Marrubium vulgare L.) in western Mediterranean cies (44%), 8 oligophagous species (30%) and 7 monophagous species (26%). At the Europe and Morocco: potential for biological control larval stage, there were five root-feeding in Australia species (22%), one stem-boring species (4%), nine leaf-feeding species (39%), eight flower, ovary or seed feeding species A Jean-Louis Sagliocco , Keith Turnbull Research Institute, Victorian (34%). Based on adult feeding behaviour Department of Natural Resources and Environment, CRC for Weed there was one root-boring species (74%), Management Systems, PO Box 48, Frankston, Victoria 3199, Australia. six leaf-feeding species (40%) and eight A Previous address: CSIRO European Laboratory, Campus International de species feeding on flowers or ovaries or Baillarguet, 34980 Montferrier sur Lez, Cedex, France. seeds (53%). Wheeleria spilodactylus (Curtis) Summary were preserved. Immature stages were (Lepidoptera: Pterophoridae) Marrubium vulgare L. (Lamiaceae) was kept with fresh plant material until the Wheeleria spilodactylus was abundant at surveyed in western Mediterranean Eu- adult stage for identification. Insects most sites in France and Spain, and had rope and Morocco to identify the phy- were observed either in the field or the been recorded feeding on M. vulgare tophagous insect fauna associated with laboratory to confirm that they fed on the (Gielis 1996) and Ballota nigra (Bigot and this weed and to select species having plant. Insects were sent to museum spe- Picard 1983). The insect’s distribution in- some potential as biological control cialists for identification and literature cludes Western and Continental Europe, agents. Twenty-seven insect species searches were conducted to assess their British Islands, the Mediterranean region, were found to feed on the plant. Two plant host-range. Selection of candidate Asia Minor and Northern Africa (Savela Lepidopteran species have been intro- biological control agents was based on 1999a). Females lay eggs underneath the duced into Australia to control the weed. their supposed degree of specificity, their leaves and the green larvae feed on leaves, Five additional species (three Lepidop- known host-plants from the literature and stems and tips of shoots, often causing tera and two Coleoptera) are considered feeding behaviour. Priority was given abortion of buds, and pupae can be found as potential candidates for introduction to insects having the strongest observed on leaves. It was the first candidate insect and host-specificity tests. impact on plants, either through plant to be considered for the biological control biomass reduction (in the case of larvae of horehound. A first consignment of lar- Introduction feeding on leaves) or through reduction in vae originating from Cap d’Agde, Herault Marrubium vulgare L. (Lamiaceae) is an in- the plant’s reproductive capacity. (43°32’N, 003°51’E) was sent to Keith vasive weed of pastures and natural habi- Turnbull Research Institute, Frankston, in tats in southern Australian states. The ge- Results 1991 for host-specificity tests, and subse- nus Marrubium comprises of 48 species, all Insect abundance quently M. vulgare was shown to be the originating from Eurasia (Seybold 1978). Significant populations of M. vulgare were preferred host-plant of the insect (J. Weiss In Europe the genus Marrubium includes found on calcareous soils with little or unpublished data). W. spilodactylus was twelve species (Tutin et al. 1972). M. no plant competition and with occa- released at many sites in Victoria and at vulgare L., an erect perennial herb, is the sional or regular grazing by sheep. In six Wyperfeld National Park in 1994 (Weiss most common species being present in all countries 55 M. vulgare populations were 1996) and later in South Australia, ACT regions but the most northern countries. examined (Table 1), and 27 insect species and Tasmania (Wills 1998). To tackle M. vulgare is also common in north Africa (Parsons and Cuthbertson 1992). It is found mostly on well-drained calcareous soils and is more common on lands where grazing occurs. In this paper, I present the results of surveys for phytophagous insects that could be used as biological control agents against M. vulgare in Aus- tralia.

Methods Horehound populations were regularly surveyed around Montpellier, southern France. Plants were randomly collected and taken to the laboratory for measure- ments and dissection. Outside of France, searches were conducted in regions with suitable alkaline soils and climate, with searches mostly done along roadside populations and on lands close to roads. Surveyed countries were Spain, Portugal, Morocco in 1991–97 with minor searches made in Italy and the former Yugoslavia in 1991 (Figure 1). Plants were randomly collected and dissected in the field. Adult Figure 1. Marrubium vulgare L. populations surveyed in western Europe and insects found on plants or after sweeping Morocco. 22 Plant Protection Quarterly Vol.15(1) 2000 climatic differences occurring within the Meligethes spp. and Meligethes rotroui country. Easton (1952) concluded from his horehound distribution in southern Easton (Coleoptera: Nitidulidae) observations, as well as from the general Australia, a second biotype of W. spilo- The Meligethes genus in Europe comprises literature on Meligethes, that these four dactylus originating from regions of Spain about 125 species (Schenkling 1913). East- species were very likely to be specific to with long dry summers, was imported on (1955) clarified the taxonomic position horehound. M. rotroui seems to be the best into Australia in 1996. of the north African species within this adapted to the dry and warm regions of group. Four species have been described Australia because of the climate in the re- Carcharodus boeticus Rambur as associated with horehound (Easton gions where it occurs in Morocco. Like the (Lepidoptera: Hesperiidae) 1952), but the small size of insects and the three other Meligethes species mentioned Carcharodus boeticus was common in small taxonomic features used for identifi- above, M. rotroui overwinter as adults and France and Spain where it was found at cation make the sorting of species difficult in Morocco becomes active on horehound most of the sites. According to Rungs and uncertain. Both adult and larval stages plants when flowers are first produced, in (1979) this species is absent from Morocco. feed on M. vulgare flowers and pollen and March. Adults feed on the flowers espe- In France, adults were observed flying in destroy significant numbers of seeds. cially on pollen and anthers. After suffi- April, June and September and larvae The distribution of M. nanus in France cient food intake they become sexually have been recorded on M. vulgare and extends from the Perpignan region to Pro- mature, mate and lay eggs on the flower Ballota foetida Lamk. (Lhomme 1935, vence Easton (1951), and the species is also clusters. Larvae hatch and develop in the Savela 1999b). Larvae are nocturnal and found in Spain (Schenkling 1913). M. calyxes, feeding on pollen and ovaries, feed on horehound leaves, hiding during tropicus occurs in southern France, Spain moving from flower to flower to complete the day in a nest made with rolled leaves and along the coastal areas of North Af- their development. Gradually, adults spun with silk. This species was consid- rica (Reitter 1919), while the distribution from the previous generation die, and ered to be a potential agent for horehound of M. villosus extends from Germany to fully developed larvae pupate in the soil and sent to quarantine in Australia in 1994 Morocco. The species M. rotroui was de- litter at the base of plants in April. In May, and 1995. However the introduction was scribed by Easton (1952) after close exami- adults of the new generation can be found unsuccessful due to difficulties in obtain- nation of specimens from Morocco, ini- on plants were they feed until early June, ing matings in quarantine. No further at- tially identified as M. villosus or M. trop- before they disperse, probably into the tempt has been made with this species. icus. His conclusion was that M. villosus woodlands where they aestivate during was the commonest species to occur in this the dry summer. Chamaesphecia mysiniformis (Boisduval) (Lepidoptera: Sesiidae) Table 1. Countries and number of Marrubium vulgare populations surveyed. Chamaesphecia mysiniformis was found in northern Spain, around Zaragoza Country Years No. M. vulgare No. insect species (Aragon Province) where the largest hore- populations found hound populations occur. According to France 1991–97 15 24 Lastuvka and Lastuvka (1995) and Leraut Spain 1991–97 20 18 (1997) the insect is present in France but Portugal 1991–92 2 4 was not found during this study. In Mo- Italy 1991 5 2 rocco its status is not clear. Rungs (1979) Former Yugoslavia 1991 2 7 does not mention it, while Savela (1999c) Morocco 1993–97 11 11 reports its presence, but it was not found in Morocco during this study. C. mysini- Total – 55 – formis has one generation per year, fe- males laying eggs at base of plants in June 30 in Spain. Larvae develop in roots of ma- nCandidate candidate agents ture plants generally causing death of the nPolyphagous polyphagous insects plant, sometimes before the adult emer- allAll insects insects gence, or during the following year. Due 25 to the damage observed in the field, and its probable host-specificity, this species was considered to have a strong potential 20 as a biological control agent. Biology and host-specificity of the insect were studied at CSIRO European Laboratory (Sagliocco 15 and Coupland 1995) and approval was given by the Australian Quarantine and No. of species Inspection Service and Environment Aus- 10 tralia to import C. mysiniformis as eggs into quarantine in 1995. However the transfer of the insect from the northern to the 5 southern hemisphere posed several prob- lems. A temperature protocol was estab- lished to allow re-synchronization of the 0 insect in quarantine during larval devel- 0102030405060 opment, and reduction of its life cycle from twelve to seven months allowed No. of M. vulgare populations emergence of adults during the Australian summer. Initial releases were made in Figure 2. Increase in number of insect species found with number of 1997 and further releases should occur in Marrubium vulgare populations surveyed (France =15, Spain =20, Portugal southern Australia in 1999. =2, Italy =5, former Yugoslavia =2, Morocco =11). Plant Protection Quarterly Vol.15(1) 2000 23 Table 2. Insects collected feeding on M. vulgare. Collected in countryB Plant assoc.C Species RFA (number of sites) (larva),[adult] HSD References Coleoptera: Buprestidae Trachys goberti (des Gozis) R F (3), S (2) (I–R) O Therond 1975 Coleoptera: Cerambycidae Phytoecia melanocephala Fabricius LC M (6) (I–R) M Villiers 1946 Phytoecia virgula (Charpentier) R F (1) (I–R) P Villiers 1978 Coleoptera: Chrysomelidae Chrysomela banksi Fabricius LC F (9), S (1), Y (1) (E–L), [E–L] O Balachowski 1963, Therond 1976 Longitarsus ballotae (Marsh.) LC F (7), S (6), I (1), M (2) (E–L), [E–L] O Therond 1976 Coleoptera: Mordellidae Mordellistena sp. LC F (9), S (5), I (3) (I–S) P Therond 1975 Coleoptera: Nitidulidae Meligethes nanus Erichson R F (3), S (2) (E–S), [E–S] M Easton 1952, 1955 M. tropicus Reitter LC F (2), S (5), Y (2), M (10) (E–S), [E–S] M Easton 1952, 1955 M. villosus Brisout LC F (3), S (2), Y (2), M (10) (E–S), [E–S] M Easton 1952, 1955 M. rotroui Easton A M (11) (E–S), [E–S] M Easton 1952, 1955 Coleoptera: Phalacridae Olibrus bisignatus (Ménétriès) R F (1), M (1) (E–S) P Diptera: Anthomyiidae Delia platura (Meigen) LC F (3), S (4), Y (1) (E–L) P Hennig 1976 Diptera: Cecidomyiidae unidentified species LC F (4), M (1) (E–S) O* Diptera: Tephritidae Aciura coryli (Rossi) R F (6), S (1), Y (1) (E–S) P White 1992 Embioptera: Embiidae Embia ramburi Rimsky-Korsakow R F (4), S (6) (E–R), [E–R] P* Homoptera: Aphididae Aphis ballotae (Passerini) LC F (5), S (1) (E–L, St) M Tuatay and Remaudière 1964 Homoptera: Cicadellidae Eupteryx melissae (Curtis) LC F (7), S (6), M (2) (E–L), [E–L] P Alford 1994, Ribaut 1936 Heteroptera: Tingidae Tingis (Neolasiotropis) marrubii Vallot LC F (12), S (4), P (1), (E–L),[E–L] M Péricart 1983 Y (2), M (4) Hymenoptera: Formicidae Messor barbara (L.) LC F (4), S (1) [S] P Aphaenogaster senilis (Mayr) R P (1) [S] P Camponotus cruentatus Latreille R F (1), P (1) [S] P Tapinoma nigerrimum (Nyl.) R F (1) [S] P Lepidoptera: Hesperiidae Carcharodes boeticus Rambur C F (12), S (20), P (2) (E–L) O Savela 1999 Lepidoptera: Pterophoridae Wheeleria spilodactylus (Curtis) A F (13), S (20), P (2), (E–L, B) O Bigot and Picard 1983, Rungs 1979 I (1),Y (1), M (2) Lepidoptera: Sesiidae Chamaesphecia mysiniformis (Boisduval) A S (8) (I–R) O Sagliocco and Coupland 1995, Lastuvka and Lastuvka 1995, Savela 1999 Lepidoptera: Tortricidae Endothenia pauperculana Staudinger LC F (5), S (2) (E–B, F, S) O Lhomme 1935 Thysanoptera: Phlaeothripidae Haplothrips reuteri (Karny) LC F (14), S (3) (E–L), [E–L] P Lewis 1973 A Relative frequency: A = abundant (found at most sites, often in large numbers), C = common (found at many sites but not abundant), LC = locally common, R = rare. B Collected in country: F = France, I= Italy, M= Morocco, P= Portugal, S = Spain, Y = former Yugoslavia. C Plant association: B = bud, E = external feeding, F = flower, I = internal feeding, L = leaf, S = seed, St = stem, R = root. D Host specificity: M = monophagous, only feeding on M. vulgare, O = oligophagous, feeding restricted to plants within the Lamiaceae, P = polyphagous, * = status unknown. 24 Plant Protection Quarterly Vol.15(1) 2000 Meligethes rotroui is thought to have a back to the CSIRO quarantine facilities at seed’s abortion. No Cecidomyiid has been strong potential for the biological control Baillarguet for rearing and observations. recorded so far on horehound from France of M. vulgare through seed number reduc- In spite of precautions taken during trans- (Dauphin and Aniotsbehere 1993) and the tion. Another species of Meligethes, M. portation, all insects died within eight insect could not be identified, suggesting planiusculus has been imported for the bio- days, suggesting a very short adult life- that this species is still undescribed. logical control of Paterson’s curse (Echium span, a feature which seems to be a com- plantagineum) and in a field experiment mon within this genus (C. Cocquempot Lepidoptera: Sesiidae caused a 65% reduction of seeds produced personal communication). However, tech- Two other insects are mentioned in the lit- (Swirepik et al. 1996). nical difficulties related to the biology of erature, but were not found during this A first consignment of M. rotroui was the insect, such as egg-laying (females lay survey. The Sesiid, Chamaesphecia maurusia sent to Australia in April 1997. Insects eggs inside the lower part of stems) and Püngeler is reported on Marrubium spp. were collected in March in the Meknes re- the short adult longevity pose problems in Algeria, Morocco and Spain (Savela gion, Morocco and sent to Montpellier for collections in northern Africa and ship- 1999c). The Sesiid, C. oxybeliformis then to Melbourne but unfortunately all ment to quarantines laboratories for fur- (Herrich-Schäffer), is reported from M. insects were dead on arrival, possibly be- ther studies, either being in Australia or in vulgare and M. peregrinum (Lastuvka and cause they were collected too early and France. Lastuvka 1995, Savela 1999c) from Mac- did not have time to build fat reserves, edonia, Greece, the Balkan region and thus losing vigour during transportation. Other insects Asia Minor. These insects may have some Further collections should be carefully Endothenia pauperculana Staudinger potential for the biological control of M. timed to allow shipments of insects in (Lepidoptera: Tortricidae) (=Enarmonia vulgare, especially if their fecundity is good condition before their peak in egg- nougatana Chrétien) higher than C. mysiniformis. laying. In France this species is restricted to the southern region and has several genera- Discussion Phytoecia melanocephala Fabricius tions between spring and autumn. Larvae This study on the horehound insect fauna (Coleoptera: Cerambycidae) develop on buds, flowers and seeds of has shown that all parts of the plant are The genus Phytoecia includes many spe- horehound and Sideritis hirsuta (Lamia- attacked by specialist insects and that cies throughout the Palaeartic region but ceae) (Lhomme 1935). This insect was not some possibilities of biological control ex- only a few species in western Africa. found in large numbers, however because ist with two insect orders, Lepidoptera Villiers (1946) records the presence of P. of its host-plant range this species may and Coleoptera. Two lepidopteran species melanocephala in northern Africa (Mo- deserve further consideration. have already been introduced into Aus- rocco, Algeria, Tunisia) and Sicily. Adults tralia. One species (W. spilodactylus) is well are diurnal and larvae develop in stems Aphis ballotae (Passerini) established, has been widely distributed and root. The discovery of larvae of P. (Homoptera:Aphididae) and has an impact on the horehound melanocephala developing in M. vulgare Aphis ballotae was locally common in plants. The second lepidopteran (C. roots was the first record of this insect’s France, occurring in small colonies on mysiniformis) is not yet established, but re- larval host-plant. In Morocco, P. melano- some individual plants. According to cent results are encouraging. Concerning cephala was the only root-borer found in Tuatay and Remaudière (1964) A. ballotae coleopteran insects, some potential exist horehound roots. Plants collected on is common in horehound in central Eu- with the pollen and seed-feeder M. rotroui, roadsides at El Haj-Kaddour in the rope and in northern Iran, though Stroyan which may help to significantly reduce Meknes region in March 1994, had 41% (1984) mentions uncertainties about status seed set and recruitment, making this in- attack by P. melanocephala (Sagliocco un- of the species and host-plants. Without sect the next candidate agent to import published data). P. melanocephala was also field observations in other regions of Eu- into Australia. The root-borer, P. melano- recorded at Bir-Tam-Tam (Taza), Meknes, rope where the insect may have a stronger cephala will have a similar effect as C. Mohammedia (Casablanca) and Azilal impact and a clearer status of this taxon, it mysiniformis but collection and host- (Beni-Mellal). The most serious damage is difficult to consider A. ballotae as a po- specificity tests pose technical problems. was observed at Meknes and at Moham- tential biological control agent for hore- Another lepidopteran species, E. pauper- media, where a horehound population hound. culana, may have some potential and identified in 1994 had few surviving could complement seed control offered by plants in 1996 and dissected plants show- Longitarsus ballotae (Marsham) M. rotroui. Two other sesiid insects are ed evidence of P. melanocephala damage. (Coleoptera: Chrysomelidae) known from the literature from regions in Adults emerge in May–June and can be Longitarsus ballotae was locally common in Europe climatically comparable to Aus- found on horehound stems where they France and Spain. Adults feed on leaves tralia. They may be specific to horehound feed and mate. Adult life-span seems to be making shot-holes and larvae feed on and could be considered as potential short, not exceeding two or three weeks roots of horehound seedlings and young agents to be imported if further searches and adults have also been observed feed- plants. Insect’s impact appears to be mini- in northern Africa and the Aegean region ing on horehound stems in cages, and on mal. are considered necessary. thistles capitula in the wild (Villiers 1946). The larvae develop within the root, even- Tingis marrubi Vallot (Heteroptera: Acknowledgments tually causing death of the plant and the Tingidae) This work was jointly funded by CSIRO life-cycle is possibly completed in one Tingis marrubi is probably specific to M. Entomology, the Wool Research and De- year. Field surveys suggest that P. melano- vulgare (Péricart 1983), but this insect was velopment Corporation, the Keith cephala is restricted to horehound. Its dis- never found to be abundant on hore- Turnbull Research Institute, the CRC tribution shows a likely adaptation to high hound. Adults and larvae feed on leaves Weed Management Systems and the summer temperatures, which rise to over cells and cause local depigmentation. South Australian Animal and Plant Con- 40°C in the Meknes region. A second col- trol Commission. C. Ziegler and Andi lection of insects was made in June 1996 at Unidentified Cecidomyiidae Walker are gratefully acknowledged for Aïn-Toto (18 km east of Meknes), with 290 This species was never found to be abun- their work. I wish to thank the following adults collected by sweeping while resting dant. Larvae develop in the calyx on the scientists who provided identification of or mating on horehound plants, and taken ovary and provoke its deformation and the insects: Professor L. Passera (CNRS, Plant Protection Quarterly Vol.15(1) 2000 25 Toulouse) Hymenoptera, Formicidae, M. 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