Past and present initiatives on the biological control of camara () in

J-R. Baars & S. Neser ARC - Protection Research Institute, Private Bag X134, Pretoria, 0001 South Africa

Lantana camara, a highly invasive weed in many countries, has been targeted for biological control in South Africa since the early 1960s. An earlier review in 1991 indicated that, despite the establishment of several natural enemy species, the programme has largely been unsuccessful. In this paper we review initiatives undertaken during the 1990s and discuss (i) the status of the natural enemies established on the weed, (ii) factors that have limited the impact of these agents, (iii) the potential of eleven new biocontrol candidates currently under evaluation for re- lease and (iv) the problem of expanded host ranges of imported natural enemies under labora- tory conditions. Ultimately, the success of the programme will depend on the establishment of a suite of natural enemies, attacking several parts of the weed, which are able to cope with the ex- treme variability and wide distribution of L. camara in South Africa. Despite the problems associ- ated with the programme, L. camara remains a candidate for biological control in South Africa. Key words: , varieties, biological weed control, natural enemies, host-specificity testing, .

Lantana camara sensu lato (Verbenaceae; Fig. 1), a compounds, notably the pentacyclic triterpenes floriferous, prickly, thicket-forming , which (Kellerman et al. 1996), lantadene A and B (Morton is commonly known as lantana, originates from 1994), which if consumed can cause photosensiti- tropical and subtropical South and Central Amer- zation, liver and kidney damage, paralysis of the ica (Stirton 1977). As a popular ornamental plant, gall bladder, intestinal haemorrhage and death several varieties (cultivars) of lantana have been within 1–4 days in cattle, sheep and horses. Live- widely distributed throughout the tropics, sub- stock previously exposed to lantana are less likely tropics and warm temperate regions of the world. to suffer from the acute symptoms caused by Following its worldwide introduction, lantana has ingestion, while those with no previous exposure become naturalized in some 50 countries and is are likely to be severely affected. The expected rated as one of the world’s worst weeds (Holm annual impact of cattle mortalities from lantana et al. 1977). poisoning in South Africa was estimated to be in Lantana is an aggressive, vigorously growing excess of R1.7 million (Kellerman et al. 1996). weed that tolerates a wide variety of environmen- Lantana is an extremely variable entity that pres- tal conditions, but thrives better in humid than in ents a complex taxonomic problem (Munir 1996). dry regions. In South Africa it is presently natural- Its conspicuous variability in general morphology ized in the warm, moist subtropical and temperate (Howard 1970; Smith & Smith 1982; Cilliers 1987a; regions (Oosthuizen 1964; Stirton 1977) of the Munir 1996), physiology and genetic composition Northern Province, Gauteng, Mpumalanga and (Spies & Stirton 1982a,b,c; Spies 1984; Spies & Du KwaZulu-Natal, as well as the southern coastal re- Plessis 1987), has led to the recognition of hun- gions of the Eastern and Western Cape Provinces dreds of cultivars or varieties, all of which are clas- (Fig. 2). Lantana invades river-banks, mountain sified as L. camara. The weed is a polyploid slopes and valleys, pastures and commercial complex, presumably derived from the deliberate forests where it forms impenetrable stands that hybridization of species in the genus Lantana obstruct access and utilization. Through allelo- (Stirton 1977) and, subsequent to naturalization in pathic suppression of indigenous plant species, South Africa, hybridization was shown to con- lantana invasions also interrupt regeneration tinue in the field (Spies & Stirton 1982a,b,c). Spies processes (Gentle & Duggin 1997a) and reduce the (1984) argued that L. camara is in an active phase of of natural . evolution, with intermediates in a transitional Lantana leaves, stems and contain toxic stage of speciation. Although the species is consid- 22 African Entomology Memoir No. 1 (1999): 21–33 50 mm

Lantana camara. (Drawn by R. Weber, National Botanical Institute, Pretoria.) ered to be unstable, certain varieties dominate in strategy (Gentle & Duggin 1997b). However, the localized areas and remain relatively stable in use of fires is not always a suitable option as infes- space and time. Following ecological disturbances, tations are often close to, or in, indigenous forests, lantana stands may recolonize as a mixture of vari- grazing lands and plantations. The difficulties and eties, but soon revert to the former dominant con- expenses incurred by conventional control mea- dition (Spies & Du Plessis 1987). sures have fostered the hope that biological con- Chemical and mechanical control of lantana was trol may provide a solution. reviewed by Cilliers & Neser (1991) who con- The biological control programme, including cluded that, although very effective, these meth- previously introduced natural enemies on L. ods are often labour-intensive and expensive. camara in South Africa, was reviewed by Cilliers & These control measures usually offer only tempo- Neser (1991), while other aspects of the weed were rary relief unless continual follow-up treatments reviewed by Swarbrick et al. (1995) and Munir are used. Controlled low- to moderate-intensity (1996). In this paper we mainly review biocontrol fires appear to reduce invasions by lantana, and initiatives undertaken during the 1990s, notably (i) can be an effective, preventative management the status of the natural enemies previously estab- Baars & Neser: Biological control of Lantana camara 23

Distribution of Lantana camara in South Africa. (Drawn by L. Henderson, Plant Protection Research Institute, Pretoria.) lished on lantana, (ii) the factors that have influ- The third species, the noctuid Neogalea enced the efficacy of these natural enemies, (iii) sunia (Guenée) (= N. esula (Druce), failed to estab- new biocontrol candidates under evaluation for lish despite introductions from Trinidad in 1962 release in South Africa and (iv) the problem of and 1968 and later from in 1983 (Cilliers expanded host ranges of natural enemies under & Neser 1991). The remaining two species, laboratory conditions. haemorrhoidalis Guenée and Teleonemia scrupulosa Stål became established following the initial re- STATUS OF NATURAL ENEMIES leases (Table 2). ESTABLISHED IN SOUTH AFRICA Although widely established in South Africa, the Biological control of lantana in South Africa was -feeding pyralid, S. haemorrhoidalis, occurs initiated during 1961/62, with the introduction of mostly in low numbers and its impact on the weed five natural enemy species (Oosthuizen 1964). is unknown. By contrast, the sap-sucking lace bug, However, two of these, laceratalis Walker T. scrupulosa, has become widely established in (= H. strigata (F.)) and lantanae high numbers throughout the range of L. camara in (Froggatt), were already established in South Af- South Africa. It is uncertain whether the later im- rica (Table 1) and were misidentified during a portation and release of additional genetic mate- pre-introductory survey conducted by Oost- rial from various countries (Table 2) has influenced huizen (1964). The leaf-feeding moth Hypena the efficacy of the tingid in South Africa (Cilliers & jussalis Walker was subsequently found to be syn- Neser 1991). Feeding damage is often extensive, onymous with H. laceratalis, while specimens of O. causing periodic defoliation of L. camara popula- lantanae were misidentified as O. rhodesiensis tions, with damaged suffering reductions in Spencer, which had been described from Zimba- set (Cilliers 1983, 1987a). Tingid populations bwe (Cilliers & Neser 1991). is and their resultant damage peak in mid-summer widespread and damages seedlings and new but rapidly decline towards winter. Teleonemia growth in summer (Table1). is scrupulosa is considered to be the most effective widespread and abundant, but has little impact on natural enemy of lantana in South Africa at present. seed viability (Cilliers & Neser 1991) (Table 1). Two leaf-mining hispine beetles, Octotoma 24 African Entomology Memoir No. 1 (1999): 21–33

Status of natural enemies present on Lantana camara in South Africa prior to the initiation of the biological control programme (‘generalists’ not included).

Order/Family Natural enemy species Mode of attack Status Limitations

Diptera Ophiomyia lantanae (Froggatt) miner Widely established and abundant Low impact on seed viability; heavy parasitism Noctuidae Hypena laceratalis1 Walker Leaf chewer Widely established with considerable Larvae are only active during late damage to seedlings and new growth. summer and autumn and are often Also attacks native Lippia and Priva parasitized species Lantanophaga pusillidactyla1 Flower, fruit and Widely established, but present in low Low abundance and possible (Walker) seed chewer numbers. Also attacks native Lippia high levels of parasitism species Tortricidae Epinotia lantana1 (Busck) Flower-peduncle Widely established Unknown and shoot-tip borer Gracillariidae Cremastobombycia lantanella1 Leaf miner Widely established, but present in low Heavy parasitism Busck numbers. Attacks native Lippia species

1: scrutiny of identifications, also of specimens from indigenous plants, required. scabripennis Guérin-Méneville and Uroplata girardi (Table 2) but its effect on the established popula- Pic, released in the early 1970s (Cilliers & Neser tions is unknown. The impact of C. lantanae 1991), have become established and coexist in the populations on lantana infestations is unknown, moist, subtropical areas of the country (Table 2). but is reduced by the extensive larval parasitism Uroplata girardi, although present in Mpumalanga observed throughout the ’s range. and the Northern Province, is most successful in Besides the three species already mentioned, a the coastal regions of KwaZulu-Natal Province, further two were released in South Africa where it is widely established and reaches high but were later found to have already been estab- population densities. By contrast, O. scabripennis is lished (Table 1). Both were introduced via most abundant at inland sites, where populations in 1984 (Cilliers & Neser 1991; Julien & Griffiths peak infrequently in localized areas. Populations 1998) and neither has inflicted appreciable of both species reach damaging levels during damage on the weed. Larvae of the plume moth mid-summer and often cause the defoliation of Lantanophaga pusillidactyla (Walker) feed on the lantana stands (Cilliers 1987b), but the plants may bases of the , binding them together. Feed- recover rapidly. Although a third leaf-mining ing damage causes a typical streak of aborted flow- beetle, Octotoma championi Baly, failed to establish ers among the cluster, leaving the other flowers to after releases in 1978 (Cilliers & Neser 1991), fur- develop normally (Perkins & Swezey 1924). ther releases were made at an inland, low altitude Larvae of the tortricid moth Epinotia lantana site near Nelspruit (Mpumalanga Province) in (Busck) attack the flowers, hollowing out the 1995. The population persisted in low numbers for receptacle, and also burrow into the young shoot the following two seasons, but its present status is tips (Perkins & Swezey 1924). unknown (Table 2). Although never deliberately introduced, the The leaf-mining fly, lantanae (Frick), tineid moth Cremastobombycia lantanella Busck is released in 1982 (Cilliers & Neser 1991) has also be- widely established in South Africa (Table 1). The come widespread (Table 2). Populations initially larvae initiate serpentine leaf mines, which later established in the warm, subtropical regions and develop into ‘blister’mines, and later pupate in subsequently became widely established in the spindle-shaped, ribbed cocoons, which are sus- temperate regions. The blotch mines initiated by pended within the ‘blisters’. Populations are the appear more abundant in the subtropical usually low, suffer heavy parasitism, and also regions, with most of the damage visible on ac- cause negligible damage to lantana. Moths be- tively-growing plants, seedlings and coppice lieved to be C. lantanella and L. pusillidactyla have growth. Additional material was released in 1989 been reared from different indigenous Lippia Baars & Neser: Biological control of Lantana camara 25

Status of natural enemies released and established on Lantana camara in South Africa.

Order/ Natural enemy species Origin Main Mode of Status Damage inflicted Family releases attack

Coleoptera Chrysomelidae Octotoma scabripennis Mexico via 1971 Leaf miner Established in the warm, moist Extensive defoliation, Guérin-Méneville Hawaii via eastern range of lantana. Abun- but localized Australia dant in localized inland areas Octotoma championi Costa Rica via 1978 Leaf miner Persisted in low numbers for two Unknown Baly Australia 1995 seasons after the last release. Establishment unconfirmed Uroplata girardi Pic Paraguay via 1974 Leaf miner Abundant in KwaZulu-Natal Extensive defoliation in Hawaii via 1983 coastal regions. Present in low coastal regions Australia numbers in the warm, moist inland range of lantana Diptera Agromyzidae Calycomyza lantanae Trinidad via 1982 Leaf miner Widely established in low Unknown (Frick) Australia numbers. Heavily parasitized Florida, USA 1989 Tingidae Teleonemia scrupulosa Mexico via Flower and Widely established in large numbers Complete defoliation and Stål Hawaii 1961 leaf sucker across the entire range of lantana; abortion of flowers in via Australia 1971 severe damage sporadic subtropical regions via Mauritius 1984 Florida, USA 1989 Lepidoptera Pyralidae Salbia haemorrhoidalis Cuba via Hawaii 1962 Flower and Widely established in low numbers. Unknown Guenée fruit feeder Reared from native Lippiaspecies species. It is possible that these two species and ized in the countries of introduction. perhaps even H. laceratalis and E. lantana were in- Several natural enemies (e.g. T. scrupulosa and C. advertently introduced into South Africa together lantanae) were reported to display preferences for with lantana plants, although they may be indige- certain varieties of lantana (Radunz 1971; Harley nous. The geographic range, correct identities and & Kassulke 1974; Harley et al. 1979; Cilliers 1987b; status of the different lepidopterans associated with Cilliers & Neser 1991). In some cases (e.g. E. xantho- lantana in South Africa are in need of revision. chaeta), agents have reportedly failed to establish because of the phenomenon of varietal resistance FACTORS AFFECTING THE IMPACT OF or reduced compatibility (Cilliers & Neser 1991). ESTABLISHED AGENTS Agents from different isolated varieties of L. Despite the establishment of several natural ene- camara, or from other species such as L. tiliaefolia mies on L. camara in South Africa (Oosthuizen (Winder & Harley 1983), may thus all be consid- 1964; Cilliers & Neser 1991), the biological control ered as ‘new’ associations when deployed against programme in South Africa has had limited the plants in South Africa. Consequently, the inter- success. This has largely been attributed to the actions between the various natural enemies and genetic diversity of lantana, which has made it an the different lantana varieties are complex and extremely variable target weed. The diversity of difficult to predict. varieties presents the natural enemies with several Harley & Kassulke (1974) and Cilliers & Neser morphological and physiological barriers to utili- (1991), amongst others, have thus emphasized the zation (Cilliers 1983; Neser & Cilliers 1990; Cilliers need to import different ‘strains’ of the natural & Neser 1991). Indeed, the introduced complex of enemies already released, so as to increase the L. camara is a man-made polyploid entity (Stirton number of lantana varieties attacked. However, 1977), which is far removed from the parent the distinction must be made between agents species occurring in its native range. Introduced previously established and those that failed to natural enemies are therefore poorly adapted to establish. Since little is known about the extent to cope with the diversity of ‘new’ entities natural- which established agents have realized their 26 African Entomology Memoir No. 1 (1999): 21–33 potential, importations of new genetic material American countries it causes ‘crinkle’ galls on the (e.g. T. scrupulosa) may not necessarily alter an leaf surface (Flechtmann 1973). In Central America agent’s status in South Africa. Unless the impacts it distorts flower buds into galls of established natural enemies are well quantified, comprising a mass of tiny green leaves (Keifer & it seems inappropriate to introduce new material. Denmark 1976). These two symptoms are geo- Neser & Cilliers (1990) highlighted the difficulties graphically distinct and seldom coexist, with of monitoring new genetic material in large, reported incidences of both kinds of symptoms well-established populations, which may result in from Florida (Cromroy 1983), Mexico (Palmer & inconclusive evidence unless suitable techniques Pullen 1995) and Venezuela. Although regarded are used. By contrast, the re-importation of new as morphologically identical, mites inducing the ‘strains’ of species that failed to establish, collected two symptoms appear to be distinct and may from different species in the lantana complex and constitute separate biotypes or species. from climates that match target release sites, is The lantana inflorescence mite was first imported expected to improve the chances of establishment from Florida, USA (Craemer 1989). Although (Neser & Cilliers 1990; Cilliers & Neser 1991). attempts to rear the mite on local lantana varieties To increase the number of lantana varieties in quarantine were largely unsuccessful, develop- attacked in South Africa, Neser & Cilliers (1990) ing colonies induced limited symptoms. In 1996, a suggested that local varieties should be exposed to colony was initiated from rooted material im- the natural enemies within the native range of L. ported from Florida, but later died out as succes- camara. This would afford several advantages but sive daughter plants were severely damaged by would depend on detailed comparative perfor- excessive gall formation. Mite-induced galls mance studies on the South African varieties. These appear to act as metabolic sinks, but also form in would indicate the natural enemies that can cope place of flowers and thereby primarily reduce seed with the different varieties as well as the degree of set. Heavy infestations of the inflorescence mite suitability of their ‘new’ hosts. observed in Florida, USA, after an exceptionally High rates of parasitism in the field have been wet season in 1998, resulted in large stands of observed for C. lantanae, C. lantanella, O. lantanae lantana being devoid of mature flowers. Following and H. laceratalis and appear to significantly re- introductions from several countries (Table 3) in duce the efficacy of these natural enemies in South 1997, a mixture of flower gall mite colonies devel- Africa. Eutreta xanthochaeta is also known to be oped characteristic symptoms on several South heavily parasitized in other countries where it has African and Australian lantana varieties in quaran- established (Daun & Messing 1996), suggesting tine (Urban, unpubl.). Successful gall induction that the recruitment of native generalist appears to require a combination of suitable parasitoids may have contributed to its failure to physiological (differentiating flower buds on an establish in South Africa. However, the possibility actively-growing plant) and environmental condi- of heavy parasitism by native parasitoids should tions (high humidity) during infestation. Host- not deter releases of new species or ‘strains’ of nat- specificity screening is underway. Additional ural enemies. Parasitized populations could still material was imported from Mexico and Vene- inflict significant damage, provided that the popu- zuela in 1998 (Table 3), in an attempt to boost the lations are able to proliferate and survive seasonal genetic base of the laboratory culture. and other adversities. Falconia intermedia (Hemiptera: Miridae) NEW BIOCONTROL CANDIDATES Two separate laboratory cultures of Falconia UNDER EVALUATION intermedia (Distant) were collected in Jamaica in The biology, host specificity and potential of 1994 and in Guatemala in 1997 (Neser, unpubl.). several species that are being evaluated for re- This species is endemic to Central America where lease in South Africa (Table 3) are summarized it is associated with several species in the L. camara below. complex (Palmer & Pullen 1995, 1998). Adults and nymphs are highly active and Aceria lantanae (Acari: Eriophyidae) mobile, and feed on the undersides of leaves. The eriophyid mite, Aceria lantanae (Cook), is Feeding damage causes chlorosis, characterized known to cause two characteristic kinds of by the stippling of the upper leaf surfaces, and can damage to Lantana species in South and Central cause them to desiccate and abscise. Eggs are America (Flechtmann & Harley 1974). In South deposited singly or in small groups, on the Baars & Neser: Biological control of Lantana camara 27

Status of biocontrol candidates recently evaluated for release on Lantana camara in South Africa.

Order/ Natural enemy species Date Origin Status Family imported

Acari Eriophyidae Aceria lantanae 1989 Florida, USA. Imported for culturing on local lantana varieties and undergoing (Cook) 1996 Florida, USA; biological studies 19971 Florida, USA. Jamaica; New material imported as separate ‘strains’ to determine Mexico compatibility with local lantana varieties. Undergoing host- 19981 Mexico; Venezuela specificity tests Hemiptera Miridae Falconia intermedia 19951 Jamaica Released in April 1999 (Distant) 19971,2 Guatemala. Imported to provide new genetic material for laboratory culture Tingidae Teleonemia vulgata 19961 Brazil Undergoing host-specificity tests Drake & Hambleton Membracidae 19951 Mexico via Australia Undergoing host-specificity tests Walker 1997 Guatemala Guatemalan culture (only) terminated Coleoptera Apionidae Coelocephalapion sp. 19971 Mexico, Cárdenas Undergoing biological studies and host-specificity screening Appears acceptable for release in South Africa 19981,2 Mexico, Veracruz Imported to provide new genetic material for laboratory culture Chrysomelidae Omophoita albicollis 1993 Jamaica Rejected because of wide host range under laboratory conditions Fabricius Culture terminated Charidotis pygmaea 19941 Colombia via Australia Undergoing performance trials on local lantana varieties for Buzzi 19981 Colombia via Australia comparison with performance on Alagoasa prob. 19971 Mexico Undergoing biological studies and host-specificity screening quadrilineata (Harold) ?Longitarsus sp. 1996 Trinidad; Florida Culture died in quarantine 1997 Mexico Culture died in quarantine 19981 Mexico, Veracruz Undergoing biological studies and developing culturing techniques ?L. columbicus Harold 19981,2 Venezuela Undergoing biological studies and developing culturing techniques Diptera Agromyzidae Ophiomyia camarae 1995 Florida, USA Culture died in quarantine Spencer 1996 Trinidad Culture died in quarantine 19971 Florida, USA; Mexico Undergoing host-specificity tests. Appears acceptable for release in South Africa 19981,2 Florida, USA New material imported to boost the quarantine culture Tephritidae Eutreta xanthochaeta 19981 Hawaii Undergoing biological studies and host-specificity tests Aldrich

1: importations from which the current laboratory cultures originate. 2: separate laboratory culture maintained. undersides of the leaves. Under laboratory condi- cantly higher rates of survival and egg production tions the eggs hatched after about 13 days and the on L. camara than on the various Lippia species. nymphs (there are five instars) completed their During multi-choice trials, L. camara was consis- development in about 14 days; adults lived for up tently selected as the preferred host plant for feed- to two months and laid about four eggs per day. ing and oviposition. Based on these results, F. Nymphs of F. intermedia completed their devel- intermedia was cleared for release, and released, in opment on L. camara and some native species of South Africa in April 1999. Lippia (Verbenaceae). No survival and develop- ment occurred on the native Lantana rugosa Teleonemia vulgata (Hemiptera: Tingidae) Thunb. or the introduced ornamental Lantana A culture of the sap-sucking lace-bug, Teleonemia montevidensis (Sprengler) Briquet, and perfor- vulgata Drake & Hambleton, was collected in 1996 mance was poor on the introduced Lantana trifolia in Rio de Janeiro, Brazil, near the only locality from L. In adult starvation trials F.intermedia had signifi- which this species was previously recorded 28 African Entomology Memoir No. 1 (1999): 21–33

(Drake & Ruhoff 1965). Damage in the field froth. The females tend the egg cases and emerg- appears similar to that caused by T. scrupulosa. ing nymphs, until these complete their develop- Several species of Teleonemia are associated with ment (Palmer et al. 1996). Nymphs undergo five the Lantana species complex in South and Central instars and display a variable rate of development, America, and some have been released as bio- ranging from 28–108 days in the greenhouse. control agents in various countries (Julien & Feeding damage causes flowers to abort and shoot Griffiths 1998). With the exception of T. validicornis tips to wilt and die back, often causing long sec- Stål (Harley & Kassulke 1971), all six Teleonemia tions of thick stems to die. species that were studied proved suitable for Host-specificity tests indicated that among the release. Teleonemia vulgata has not been previously different species of Lantana, A. compressa was evaluated as a biocontrol agent against L. camara. specific to L. camara, confirming the results of Adults and nymphs prefer to feed on flowers, Palmer et al. (1996) in Mexico and Australia. Starva- but readily feed on leaves and vegetative buds. tion tests showed that feeding on a number of Eggs are inserted singly or in small clusters into the indigenous Lippia species allowed ovariole devel- ventral veins and periphery of leaves, and into the opment, oviposition and high rates of nymphal flower peduncle. Eggs take about 14 days to hatch emergence, similar to that on L. camara. However, and the nymphs pass through five instars, taking preliminary multi-choice trials with inexperi- about 15 days to complete their development. enced adults revealed preferences for L. camara. Feeding damage results in the abortion of florets Species of Lippia may thus be able to serve as and the desiccation and abscission of leaves. marginal hosts under field conditions and further During no-choice tests, nymphs completed nor- performance and choice trials will be conducted mal development on L. camara, L. rugosa, L. trifolia, before A. compressa is considered for release in L. montevidensis, and different indigenous Lippia South Africa. species. Survival and development on the native Priva cordifolia Druce (Verbenaceae) was low, indi- Coelocephalapion sp. (Coleoptera: cating its unsuitability as a host. Preliminary adult Apionidae) starvation trials on these plant species indicated The petiole-boring apionid, an undescribed spe- that ovariole development was better on L. camara, cies of Coelocephalapion (Kissinger, pers. comm.), resulting in a higher deposition of fat reserves, was first collected in Cardenas, Tabasco Province, well-developed ovaries and eggs. During choice Mexico, during a survey in 1997, and subsequently tests, gravid females preferred to feed and oviposit at a number of sites in Veracruz, Mexico, in 1998. on L. camara, with comparatively fewer eggs de- Adults feed on the leaves of lantana, and eggs are posited on the other plant species. Additional inserted into the leaf petiole and flower peduncle. multi-choice trials are to be completed before T. Larvae burrow for a short distance into the plant vulgata may be considered for release. tissue and induce a small gall. The later instars re- main relatively sedentary and feed on callus tissue Aconophora compressa (Hemiptera: within the gall. Larvae pass through four instars Membracidae) and pupate inside the gall, and adults emerge A culture of the stem-sucking membracid, from a small exit hole chewed in the gall. The Aconophora compressa Walker, from Cuernavaca, life cycle from egg to adult is approximately Mexico, was obtained from the Queensland De- 30–35 days in the laboratory and the adults live for partment of Natural Resources, Australia, in 1995 4–5 months. Galls induced on the leaf petiole (Table 3). This species is endemic to the Neotropics disrupt the supply of liquids and may cause small (Palmer et al. 1996). Specimens collected in 1997 leaves to desiccate and abscise. Flower galls (Neser, unpubl.) in Guatemala appeared some- appear to prevent the development of in the what different from the Mexican material and a laboratory. separate quarantine culture was maintained, but Preliminary tests suggested that the weevils are later destroyed when it was confirmed to be the host specific and perform best on L. camara. same species. During starvation trials, adults fed and oviposited Adults feed on the stems of lantana and remain on the two introduced species, L. montevidensis gregarious during the pre-oviposition period. and L. trifolia, and on five indigenous species, Females then disperse to insert the eggs into namely Lantana rugosa, Lippia javanica Spreng., actively-growing stems, forming egg cases of Lippia rehmannii Pearson, Lippia wilmsii Pearson about 70 eggs that are covered by a protective and Lippia scaberrima Sond. Although a number of Baars & Neser: Biological control of Lantana camara 29 eggs were deposited on these plants during these surface. Larvae emerge from the leaf litter and trials, far fewer larvae completed their develop- feed on recently abscised leaves, or on leaves on ment on them than on L. camara. During multi- branches near the ground. Larvae pass through choice tests, adults consistently preferred to feed three instars, taking 21–25 days to complete their and oviposit on lantana. The specific oviposition development, and then burrow into the soil to behaviour of the apionid is thought to limit the pupate within a hardened chamber. In the labora- number of suitable hosts. The results so far indi- tory adults emerge from the soil after about 10 cate that the apionid may be acceptable for release days (Sparks, unpubl.). in South Africa. During starvation trials, larvae survived and developed on several species of Verbenaceae, Charidotis pygmaea (Coleoptera: including L. trifolia, several indigenous Lippia Chrysomelidae) species and Phyla nodiflora Greene. Larvae also The leaf-feeding tortoise beetle, Charidotis developed on several indigenous and economi- pygmaea Buzzi, was imported into South Africa cally important species in the Lamiaceae. During from Brazil, via Australia, in 1994 (Table 3). Adults multi-choice trials, adults fed on several species of and larvae feed on the leaves, causing characteris- Verbenaceae and Lamiaceae and caused damage tic longitudinal feeding scars on the upper leaf sur- similar to that on L. camara. The unacceptably wide faces. Eggs are deposited singly on leaves, semi- host range of O. albicollis resulted in its rejection as embedded into the lower epidermis and covered a biocontrol candidate for release in South Africa by a hardened froth excretion. Protective froth (Sparks, unpubl.) and the laboratory culture was extends from the posterior end of the egg and terminated. forms a raised covering over the egg, most likely functioning as protection against parasitoids. The Alagoasa prob. quadrilineata (Coleoptera: larvae undergo five instars, lasting about 38 days Chrysomelidae) to pupation, which occurs on the leaf surface. A supply of the leaf-feeding flea beetle, Alagoasa Although originally collected on Lantana prob. quadrilineata (Harold), was collected in tiliaefolia (Swarbrick et al. 1995), one of the closely Catemaco, Mexico in 1997 (Neser, unpubl.). Dur- related species in the L. camara complex and very ing a survey in Mexico in 1998 (Baars & Sparks similar to the weedy forms, C. pygmaea was unpubl.), similar adults were collected on mem- thought to be potentially specific to L. camara. bers of the L. camara complex in the Yucatán, However, adults performed better on the intro- Campeche, Tabasco and Veracruz provinces. duced L. montevidensis (creeping lantana) than on Adults and larvae feed on the leaves, and larvae various L. camara varieties. Survival and develop- pupate in the soil. The adults have three distinct ment also occurred on the indigenous L. rugosa colour and pattern forms (uniform, blotched and and various Lippia species, but performance was striped). Preliminary host-specificity tests indi- poor relative to that on L. montevidensis and L. cated that survival and development occurred on camara (Sparks, unpubl.). Varioussterile forms of L. closely related plants within the Verbenaceae montevidensis, and hybrids, have been introduced (Sparks, unpubl.). Alagoasa prob. quadrilineata is at into South Africa via the ornamental trade and an early stage of evaluation and further studies on are popular garden plants. The fertile form in its biology and host-specificity will be conducted Australia is regarded as invasive (Munir 1996) and before it is considered for release in South Africa. was also targeted for biological control with the release of C. pygmaea (Julien & Griffiths 1998). ?Longitarsus sp. (Coleoptera: Since C. pygmaea appears to be better suited to L. Chrysomelidae) montevidensis than to local South African lantana Adults of the flea beetles believed to belong to varieties, it seems unlikely that it will be further the genus Longitarsus were collected from Trini- considered for release in South Africa. dad and Florida in 1996 (Table 3); they failed to establish in the laboratory. A further culture of a Omophoita albicollis (Coleoptera: ?Longitarsus sp., collected in Mexico in 1997 per- Chrysomelidae) sisted for several generations in the laboratory but A culture of the leaf-feeding flea beetle, Omo- the adults did not reappear after the first winter. phoita albicollis Fabricius, was collected in Jamaica Another culture was collected from Veracruz in in 1993. Adults feed voraciously on flowers and Mexico in 1998 and still persists in the laboratory. A leaves and deposit eggs under leaf litter on the soil culture of a flea beetle, provisionally identified as 30 African Entomology Memoir No. 1 (1999): 21–33

Longitarsus columbicus columbicus Harold, was col- Eutreta xanthochaeta (Diptera: lected in Maracay, Venezuela in 1998. This species Tephritidae) was previously recorded on Lantana spp. in Vene- The stem-galling tephritid, Eutreta xanthochaeta zuela (Savini 1997). The identity and possible Aldrich, was one of the first natural enemies conspecificity of the specimens collected in the released against L. camara in Hawaii in 1902 various countries they were not determined and (Perkins & Swezey 1924). The fly was first im- were maintained as separate cultures. ported into South Africa in 1983 (Cilliers & Neser Adults of ?Longitarsus columbicus columbicus feed 1991) (Table 3) and was considered to be safe for on the leaves of lantana, and deposit their eggs in release. It was reared in quarantine for one genera- the leaf litter. Emerging larvae burrow into the soil tion and released in very low numbers at one and feed externally on secondary rootlets. Larvae site near Hartbeespoort (North-West Province). pupate in hardened cases near the soil surface. Although galls were initially recovered, the fly The immature stages require about 2 months for failed to establish, probably because too few were development in the laboratory, and the adults released, and on lantana varieties with which they lived in excess of 2 months. Reliable culture tech- may also have been incompatible (Cilliers & Neser niques are being developed before host-specificity 1991). A new culture was imported from Hawaii in tests can be conducted. 1998 and although previously released, is under- going biology studies and host-range tests in quar- Ophiomyia camarae (Diptera: antine. These tests will incorporate indigenous Agromyzidae) plant species that were not tested previously, The herringbone leaf miner, Ophiomyia camarae because of the observed tendency of other natural Spencer, originates from South and Central enemies of lantana to have expanded host ranges, America. Adult flies are small and very active, and in the light of present environmental legisla- usually inserting a single egg into the epidermal tion pertaining to biocontrol agents in South tissue on the abaxial aspect of leaves. The emerg- Africa. ing larva burrows into the mesophyll tissue, typi- Adult females insert eggs into actively-growing cally towards the midrib of the leaf. The larva then shoot tips. Larvae burrow into the stem, causing burrows laterally, in a characteristic ‘herring-bone’ the shoot to swell and form an elongated or round pattern, into the leaf lamina, and also into the gall of up to 15 mm in diameter. Rapid growth of petiole. The late instar larva usually burrows to- the apical stem above the gall is initially stunted, wards the tip of the leaf, or elsewhere near the but growth may resume after the flies emerge if edge of the leaf, where pupation occurs. Leaves the shoot tip has not died (Perkins & Swezey 1924). damaged by the larvae may abscise prematurely, Larvae feed on the proliferated gall tissue, taking and larval development is completed in abscised up to 45 days to complete development in the leaves. High populations were recorded in greenhouse. Pupation occurs within the gall, and Florida, USA (Stegmaier 1966), and were similarly adults emerge through an epidermal window pre- observed there during 1987 and 1998. pared by the larva. Characteristic leaf mines have been recorded on Preliminary quarantine tests indicate that E. L. tiliaefolia in Brazil (Winder & Harley 1983), on L. xanthochaeta oviposits on several lantana varieties, camara in Mexico (Palmer & Pullen 1995), Trinidad all of which appear suitable for larval develop- and Florida (Stegmaier 1966), on L. trifolia in Vene- ment. Oviposition and development also occurs on zuela and on unidentified Lantana species in Ja- indigenous Lippia species (Klein, unpubl.) and maica, Guatemala and Brazil. Although the performance and choice trials will be conducted identities of the flies were not all confirmed, it before further releases in South Africa are consid- appears that O. camarae is associated with various ered. species of the genus Lantana and is able to utilize them as hosts across its native geographical range. EXPANDED LABORATORY HOST Preliminary host-specificity trials confirmed this RANGES OF NATURAL ENEMIES association and the fly has performed well on Recent host-specificity tests have indicated that several local lantana varieties. Although oviposi- most of the natural enemies currently under eval- tion and larval development occurred on some uation accepted related native plant species to indigenous Lippia species, performance was far varying degrees under laboratory conditions. better on L. camara (Simelane, unpubl.) and the fly Ironically, natural enemies selected for the will be considered for release. biocontrol of lantana are required to cope with the Baars & Neser: Biological control of Lantana camara 31 variability of the weed, but are also required to not that can cope with the extreme variability and accept closely related species. Two species in the wide distribution of the weed in South Africa, genus Lantana and four in the genus Lippia consid- without compromising native Verbenaceae. It is ered native to South Africa (Arnold & De Wet apparent that the agents currently estab- 1993), are generally accepted as hosts by the re- lished on lantana in South Africa do not exert cently imported natural enemies of lantana under sufficient control and that additional natural laboratory conditions. Some insect species (e.g. A. enemies are required. In this respect, Cilliers & compressa and C. pygmaea), which were acceptable Neser (1991) suggested a possible shift in the selec- for release in Australia (Julien & Griffiths 1998), tion of new natural enemies, in which stem borers, may accept and marginally affect these non-target root feeders and flower feeders should take prece- indigenous species in South Africa. dence over leaf feeders. To reconcile physiological and true host ranges, Natural enemies established in South Africa, laboratory and field studies were conducted on notably T. scrupulosa, O. scabripennis and U. girardi, species that have been established in South Africa periodically defoliate lantana stands (Cilliers for decades. The tingid, T. scrupulosa, displayed 1987b), but fail to sustain these levels of damage to non-host specific behaviour in the laboratory, the photosynthetic niche, and thus the resource feeding and developing on a wide range of species production by the plant. This niche is therefore in within the Verbenaceae. However, preliminary need of additional herbivore pressure and new studies provided no evidence of an extended host leaf feeders should also be considered. However, range in the field where T.scrupulosa was observed several niches are not affected by natural enemy to display only limited feeding on some native attack and the suite of candidate biocontrol agents Lippia species. These studies provided further evi- should comprise species that attack as many parts dence of the conservative nature of laboratory of the plant as possible. In pursuit of this objective, tests and suggest that extended laboratory host natural enemies under consideration include ranges are often, as in many biocontrol feeders on leaves, stems, petioles and shoots, programmes worldwide, not realized under field flowerbuds and roots. The abundance of potential conditions. agents suggests that, despite the problems associ- Although some of the natural enemy species ated with the programme, L. camara remains a can- presently under evaluation (e.g. Coelocephalapion didate for biological control in South Africa. sp.) do not accept certain closely related native species, most others appear to perform well on ACKNOWLEDGEMENTS several closely related species. Aconophora compressa We thank A.J. Urban, H. Klein, H.E. Sparks, F. (Palmer et al. 1996) and T. scrupulosa (Harley & Heystek and D.O. Simelane of the Plant Protection Kassulke 1971) have been recorded on Lippia Research Institute for technical and research assis- species in their native range, but detailed perfor- tance and for the use of unpublished data. We are mance studies on other promising species (e.g. F. also grateful to M.P.Hill, T.Olckers and A.J. Urban intermedia) in the laboratory have indicated that (all of PPRI) for comments on the manuscript. We although various Lippia species are acceptable, are grateful to various organizations for providing performance was poor relative to that on L. camara. financial support for the research programme One solution to determining the acceptability of against lantana, including the National Depart- expanded laboratory host ranges would be to ment of Agriculture, Department of Water Affairs accept possible limited feeding on such non-target and Forestry, H.L. Hall & Sons, Hans Merensky species in the field, as an ecologically justifiable Foundation and the Agricultural Research Coun- ‘trade-off’ against the benefits of releasing agents cil of South Africa. that have the potential to suppress such an envi- ronmentally damaging target weed. Alternatively, REFERENCES the number of new natural enemies that will ulti- ARNOLD, T.H. & DE WET,B.C. 1993. Plants of southern Africa: names and distribution. Memoirs of the Botani- mately be considered acceptable for release in cal Survey of South Africa 62: 596–637. South Africa will be limited, with obvious con- CILLIERS, C.J. 1983. The weed, Lantana camara L., and straints on the biocontrol programme. the insect natural enemies imported for its biological control into South Africa. Journal of the Entomological CONCLUSIONS Society of Southern Africa 46: 131–138. CILLIERS, C.J. 1987a. Notes on the biology of the estab- The success of the biocontrol programme against lished insect natural enemies of Lantana camara L. lantana will depend on a suite of natural enemies (Verbenaceae) and their seasonal history in South 32 African Entomology Memoir No. 1 (1999): 21–33

Africa. Journal of the Entomological Society of Southern The distribution, diagnoses and estimated economic Africa 50: 1–13. impact of plant poisonings and mycotoxicoses in CILLIERS, C.J. 1987b. The evaluation of three insect South Africa. Onderstepoort Journal of Veterinary Re- natural enemies for the biological control of the weed search 63: 65–90. Lantana camara L. Journal of the Entomological Society of MORTON, J.F.1994. Lantana, or red sage (Lantana camara Southern Africa 50: 15–34. L., [Verbenaceae]), notorious weed and popular CILLIERS, C.J. & NESER, S. 1991. Biological control of garden flower; some cases of poisoning in Florida. Lantana camara (Verbenaceae) in South Africa. Agri- Economic Botany 48: 259–270. culture, Ecosystems and Environment 37: 57–75. MUNIR, A.A. 1996. A taxonomic review of Lantana camara CRAEMER, C. 1989. Eriophyidae (Acari) as potential L. and L. montevidensis (Spreng.) Briq. (Verbenaceae) control agents of South African weeds, with descrip- in Australia. Journal of the Adelaide Botanical Gardens 17: tions of a new species of Tegonotus Nalepa and of 1–27. Paraphytoptus Nalepa. M.Sc. thesis, Rand Afrikaans NESER, S. & CILLIERS, C.J. 1990. Work towards biologi- University, Johannesburg. cal control of Lantana camara: perspectives. In: CROMROY,H.L. 1983. Potential use of mites in biological Delfosse, E.S. (Ed.) Proceedings of the Seventh Interna- control of terrestrial and aquatic weeds. In: Hoy, tional Symposium on Biological Control of Weeds. M.A., Cunningham, G.L. & Knutson, L. (Eds) Biologi- 363–369. Istituto Sperimentale per la Patologia cal Control of Pests by Mites. 61–66. University of Vegetale Ministero dell’Agricoltura e delle Foreste, , Berkeley. Rome. DAUN, J.J. & MESSING, R.H. 1996. Response of two OOSTHUIZEN, M.J. 1964. The biological control of opiine fruit fly parasitoids (Hymenoptera: Lantana camara L. in Natal. Journal of the Entomological Braconidae) to the lantana gall fly (Diptera: Society of Southern Africa 27: 3–16. Tephritidae). Biological Control 25: 1428–1437. PALMER, W.A. & PULLEN, K.R. 1995. The DRAKE, C.J. & RUHOFF, F.A. 1965. Lacebugs of the phytophagous associated with Lantana world: a catalog (Hemiptera: Tingidae). Bulletin of the camara, L. hirsuta, L. urticifolia and L. urticoides United States National Museum 243: 1–634. (Verbenaceae) in North America. Biological Control 5: FLECHTMANN, C.H.W. 1973. On an eriophyid mite 54–72. (Acari) from lantana from Brazil. Anais da Sociedade PALMER, W.A., WILLSON, B.W. & PULLEN, K.R. 1996. Entomológica do Brasil 2: 109–110. The host range of Aconophora compressa Walker FLECHTMANN, C.H.W.& HARLEY,K.L.S. 1974. Prelim- (Homoptera: Membracidae): a potential biological inary report on mites (Acari) associated with Lantana control agent for Lantana camara L. (Verbenaceae). camara L. in the Neotropical region. Anais de Sociedade Proceedings of the Entomological Society of Washington Entomológica do Brasil 3: 69–71. 98: 617–624. GENTLE, C.B. & DUGGIN, J.A. 1997a. Allelopathy as a PALMER, W.A.& PULLEN, K.R. 1998. The host range of competitive strategy in persistent thickets of Lantana Falconia intermedia (Distant) (Hemiptera: Miridae): a camara L. in three Australian forest communities. potential biological control agent for Lantana camara Plant Ecology 132: 85–95. L. (Verbenaceae). Proceedings of the Entomological GENTLE, C.B. & DUGGIN, J.A. 1997b. Lantana camara L. Society of Washington 100: 633–635. invasions in dry rainforest-open ecotones: the role of PERKINS, R.C.L. & SWEZEY, O.H. 1924. The introduc- disturbances associated with fire and cattle grazing. tion into Hawaii of that attack lantana. Hawaii Australian Journal of Ecology 22: 298–306. Sugar Planters Association Experimental Station Bulletin HARLEY,K.L.S. & KASSULKE, R.C. 1971. Tingidae for bi- (Entomological Series) 16: 1–83. ological control of Lantana camara [Verbenaceae]. RADUNZ, L.A.J. 1971. Some aspects of the preferential Entomophaga 16: 389–410. behaviour of Teleonemia scrupulosa Stål, towards its HARLEY, K.L.S. & KASSULKE, R.C. 1974. The suitability host plant Lantana camara. Hons. thesis, University of of Phytobia lantanae Frick for biological control of Queensland. Lantana camara in Australia. Journal of the Australian SAVINI, V. 1997. Evaluación de los datos sobre los Entomological Society 13: 229–233. phytophaga dañinos en Venezuela (Coleoptera). HARLEY, K.L.S., KERR, J.D. & KASSULKE, R.C. 1979. Boletin de Entomologia Venezolana (Serie Monografias) Effects in S.E. Queensland during 1967–72 of insects 1: 95–96. introduced to control Lantana camara. Entomophaga SMITH, L.S. & SMITH, D.A. 1982. The naturalised 24: 65–72. Lantana camara complex in eastern Australia. HOLM, L.G., PLUCKNETT, D.L., PANCHO, J.V. & Queensland Botanical Bulletin No. 1. Queensland HERBERGER, J.P.1977. The World’s Worst Weeds. The Department of Primary Industry, Brisbane. University Press of Hawaii, Honolulu. SPIES, J.J. 1984. A cytotaxonomic study of Lantana camara HOWARD, R.A. 1970. Lantana camara – a prize and a peril. (Verbenaceae) from South Africa. South African Jour- American Horticultural Society Winter: 31–36. nal of Botany 3: 231–250. JULIEN, M.H. & GRIFFITHS, M.W. 1998. Biological Con- SPIES, J.J. & DU PLESSIS, H. 1987. Sterile Lantana camara: trol of Weeds: A World Catalogue of Agents and their fact or theory. South African Journal of Plant and Soil 4: Target Weeds. 4th Edition. CABI Publishing, UK. 171–174. KEIFER, H.H. & DENMARK, H.A. 1976. Eriophyes SPIES, J.J. & STIRTON, C.H. 1982a. Chromosome num- lantanae Cook (Acarina: Eriophyidae) in Florida. bers of South African plants. South African Journal of Florida Department of Agricultural Services, Division Botany 48: 21–22. of Plant Industry,Entomology Circular No. 166, 2 pp. SPIES, J.J. & STIRTON, C.H. 1982b. Meiotic studies of KELLERMAN, T.S., NAUDE, T.W. & FOURIE, N. 1996. some South African cultivars of Lantana camara Baars & Neser: Biological control of Lantana camara 33

(Verbenaceae). Bothalia 14: 101–111. of the Second National Weeds Conference of South Africa. SPIES, J.J. & STIRTON, C.H. 1982c. Embryo sac develop- 321–344. A.A. Balkema, Cape Town. ment in some South African cultivars of Lantana SWARBRICK, J.T.,WILLSON, B.W.& HANNAN-JONES, camara. Bothalia 14: 113–117. M.A. 1995. The biology of Australian weeds: Lantana STEGMAIER, C.E. 1966. A leaf miner on Lantana in camara L. Plant Protection Quarterly 10: 82–95. Florida, Ophiomyia camarae (Diptera, Agromyzidae). WINDER, J.A. & HARLEY, K.L.S. 1983. Phytophagous The Florida Entomologist 49: 151–152. insects on lantana in Brazil and their potential for bio- STIRTON, C.H. 1977. Some thoughts on the polyploid logical control in Australia. Tropical Pest Management complex Lantana camara L. (Verbenaceae). Proceedings 29: 346–362.