Prospective agents for the biological control of Tithonia rotundifolia (Mill.) S.F.Blake and Tithonia diversifolia (Hemsl.) A.Gray (Asteraceae) in South Africa
D.O. Simelane1*, K.V. Mawela1 & A. Fourie2 1Agricultural Research Council-Plant Protection Research Institute, Private Bag X134, Queenswood, 0121 South Africa 2Agricultural Research Council-Plant Protection Research Institute, Private Bag X5017 Stellenbosch, 7599 South Africa
Starting in 2007, two weedy sunflower species, Tithonia rotundifolia (Mill.) S.F.Blake and Tithonia diversifolia (Hemsl.) A.Gray (Asteraceae: Heliantheae), were targeted for biological control in South Africa. Surveys conducted in their native range (Mexico) revealed that there were five potential biological control agents for T.rotundifolia, and three of these are currently undergoing host-specificity and performance evaluations in South Africa. Two leaf-feeding beetles, Zygogramma signatipennis (Stål) and Zygogramma piceicollis (Stål) (Coleoptera: Chrysomelidae), are the most promising biological control agents for T. rotundifolia: prelimi- nary host-specificity trials suggest that they are adequately host-specific. The stem-boring beetle, Lixus fimbriolatus Boheman (Coleoptera: Curculionidae), is also highly damaging to T. rotundifolia, but its host range is yet to be determined. Two other stem-boring beetles, Canidia mexicana Thomson (Coleoptera: Cerambycidae) and Rhodobaenus auctus Chevrolat (Coleoptera: Curculionidae), have also been recorded on T. rotundifolia, and these will be considered for further testing if L. fimbriolatus is found to be unsuitable for release in South Africa. Only two insect species were imported as candidate agents on T. diversifolia, the leaf-feeding butterfly Chlosyne sp. (Lepidoptera: Nymphalidae), and an unidentified stem-boring moth (Lepidoptera: Tortricidae): the latter was tested in quarantine but rejected because it attacked several sunflower cultivars. Only one pathogen, Puccinia enceliae Dietel & Holw. (Uredinales: Pucciniaceae), was found that could potentially have been used as a biological control agent against the Tithonia species, but attempts to culture this rust were unsuccessful. Key words: red sunflower, Mexican sunflower, Zygogramma signatipennis, Zygogramma piceicollis, Lixus fimbriolatus.
INTRODUCTION Red sunflower, Tithonia rotundifolia (Mill.) Tithonia rotundifolia (Fig. 1) is a large, robust annual S.F.Blake, and Mexican sunflower, Tithonia diversi- plant and grows up to 3 m in height. The leaves of folia (Hemsl.) A.Gray (Asteraceae: Heliantheae), T. rotundifolia are often paired, each triangular-ovate, from Mexico have become invasive in the humid or sometimes deeply three-lobed, and the red- and sub-humid tropics of Central and South dish-orange flowers are held singly on long stems. America, South East Asia and tropical and sub- Tithonia diversifolia (Fig. 2) is a large evergreen tropical Africa (Lazarides et al. 1997; Meyer 2000; perennial shrub and grows up to 5 m tall, and has Varnham 2006; Henderson 2001). The increasing deeply divided, paired leaves and orange-yellow abundance of T. rotundifolia and T. diversifolia in flowers on erect, hollow woody stems. In South conservation and agricultural areas over the past Africa, flowering in T. rotundifolia occurs from ten years in South Africa has been of concern, re- late summer and throughout autumn, while sulting in the initiation of a biological control T. diversifolia flowers in autumn and winter. programme against these two species in 2007. Tithonia rotundifolia produces fewer, larger and The genus Tithonia comprises 11 species, with heavier seeds, which may explain its early and the centre of distribution in Mexico, but with one vigorous seedling growth and longer survival in species extending into the southwestern U.S.A., relatively unfavourable conditions (Muoghalu & and several species extending into some Central Chuba 2005). By contrast, T. diversifolia produces American countries (Muoghalu & Chuba 2005). numerous, smaller, lighter seeds which allow for
*To whom correspondence should be addressed. dispersal over large areas (Muoghalu & Chuba E-mail: [email protected] 2005), and T. diversifolia cuttings, buried horizon-
African Entomology 19(2): 443–450 (2011) 444 African Entomology Vol. 19, No. 2, 2011
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Fig. 1. Tithonia rotundifolia. (Drawn by W.Roux; first published in Henderson (1995), ARC-Plant Protection Research Institute, Pretoria.) tally into the soil, often sprout, contributing to the (Henderson 2001). Both T. rotundifolia and T. diver- densification of stands of this species. sifolia are aggressive colonizers, particularly in Deliberately introduced and widely cultivated disturbed, sun-exposed ecosystems, abandoned as ornamental plants, both T. rotundifolia and sites, and along railways and roads, and they are T. diversifolia have become invasive in the tropics declared Category 1 weeds in South Africa and subtropics (Lazarides et al. 1997; Meyer 2000), (Henderson 2001). including several countries in sub-Saharan Africa Although the uses of Tithonia species as medicinal (Chukwuka et al. 2007). In Nigeria, T. diversifolia is plants (Lin et al. 1993; Takahashi 1998; Tona et al. becoming an important weed of arable crops in 1998), livestock fodder (Roothaert & Paterson Oyo, Gbongan and Ogun States, forcing some 1997), poultry feed (Odunsi et al. 1996) and green farmers to abandon their lands (Chukwuka et al. manure (Nagarajah & Nizer 1982; Drechsel & Reck 2007). Following their introduction into South 1998; Jama et al. 2000) are widely acknowledged in Africa in the 1900s (Henderson 2006), both Tithonia various parts of the world, the problems they species are now invasive in KwaZulu-Natal cause in Africa as invasive weeds far outweigh (KZN), Limpopo and Mpumalanga provinces, their benefits. with T. rotundifolia extending its range into the There are no herbicides registered for the control North West and Gauteng provinces (Fig. 3) and of either of the Tithonia species in South Africa, and T. diversifolia being more abundant and wide- mechanical control is largely ineffective due to the spread along the humid and low-altitude areas ability of T. diversifolia to coppice from stems and of Mpumalanga and KZN provinces (Fig. 4) because of the rapid recruitment of seedlings of Simelane et al.: Biological control of Tithonia species (Asteraceae) 445
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Fig. 2. Tithonia diversifolia. (Drawn by W. Roux; first published in Henderson (1995), ARC-Plant Protection Research Institute, Pretoria.) both species in cleared areas. Consequently, a bio- (Jasq.) Cass, in and around Mexico City in 2007, it logical control programme was initiated, and field was later recorded on T. rotundifolia at several sites surveys for potential biological control agents in the Oaxaca and Chiapas states of Mexico. In were conducted in Mexico during 2007 and 2008 2008, Z. piceicollis was collected on T. rotundifolia (Fig. 5). Nine candidate agents were recorded on near Puerto Angel, along the humid south coast Tithonia species at over 100 sites, and eight of these region of Mexico. Zygogramma signatipennis is the were subsequently introduced into quarantine in larger of the two, and is shiny black in colour with South Africa for further evaluation. The biology, silver green markings on the elytra. Zygogramma host specificity and impact of those that were piceicollis has a dark red head and thorax with light introduced and evaluated for possible release are grey markings on the elytra. The two beetle species reviewed below in descending order of their per- have very similar life histories and feeding habits. ceived suitability as biological control agents. Females of both species usually deposit their eggs singly on the lower leaf surface, mostly along the INSECT NATURAL ENEMIES OF leaf veins, but occasionally on the flower heads. TITHONIA ROTUNDIFOLIA Adult and larval feeding by both beetle species on the leaves is highly damaging, often skeletonizing Zygogramma signatipennis (Stål) and them completely. Late-instar larvae drop from the Zygogramma piceicollis (Stål) host plant and burrow into the ground to pupate. (Coleoptera: Chrysomelidae) Development from egg to adult takes about four to The two leaf-feeding beetles, Z. signatipennis and five weeks. Z. piceicollis, are the most promising biological To determine the host range of the two Zygo- control agents for T. rotundifolia. Although gramma species, trials were initiated in 2008 under Z. signatipennis was initially collected from a quarantine conditions in South African, and in the closely-related plant species, Tithonia tubaeformis field in Mexico. Preliminary results of paired- and 446 African Entomology Vol. 19, No. 2, 2011
Fig. 3. Distribution of Tithonia rotundifolia in South Africa. (Drawn by L. Henderson; data source: SAPIA database, ARC-Plant Protection Research Institute, Pretoria.) no-choice tests indicated that both species of to black in colour, are long-lived, with combined Zygogramma strongly prefer T. rotundifolia to other pre-oviposition and oviposition periods of over closely-related plant species for feeding, oviposition 12 months. The adults nibble along the margin of and larval development. If, after further testing, the leaf and lay their eggs into the stems, approxi- they are found to be adequately host-specific to mately 4 cm above the soil surface. The larvae tun- T. rotundifolia, permission to release both beetle nel in and hollow out the stem, which could species in South Africa will be sought. Surveys in increase the vulnerability of plants to wind dam- Mexico indicate that Z. signatipennis is predominant age. The larvae are very destructive, especially in drier inland regions while Z. piceicollis is mainly when plants are attacked at an early stage of devel- found in warm, humid coastal regions, which opment. Larvae often pupate near the shoot tip, might indicate that the release of both species from where the adults emerge. Development from could result in effective control throughout the the egg to adult stage is completed in five to six distribution range of T. rotundifolia in South Africa. months. A reliable rearing technique has been developed (Mawela & Simelane 2009), and Lixus fimbriolatus Boheman host-specificity studies on this weevil have been (Coleoptera: Curculionidae) initiated. The stem-boring weevil L. fimbriolatus was col- lected from T. rotundifolia in Mexico and intro- Canidia mexicana Thomson duced into quarantine in South Africa in October (Coleoptera: Cerambycidae) 2008. Lixus fimbriolatus adults, which are dark grey Larvae of the stem-boring longhorn beetle, Simelane et al.: Biological control of Tithonia species (Asteraceae) 447
Fig. 4. Distribution of Tithonia diversifolia in South Africa. (Drawn by L. Henderson; data source: SAPIA database, ARC-Plant Protection Research Institute, Pretoria.)
C. mexicana, were found almost everywhere latus proves to be unsuitable for release against within the natural distribution of T. rotundifolia in T. rotundifolia. Mexico (Fig. 5). As in the case of L. fimbriolatus, C. mexicana adults deposit their eggs into the stem. INSECT NATURAL ENEMIES OF Upon eclosion, the larvae tunnel in the stem, TITHONIA DIVERSIFOLIA (Table 1) causing extensive damage. However, several attempts to rear the beetle under quarantine labo- Chlosyne sp. (Lepidoptera: Nymphalidae) ratory conditions were unsuccessful. A defoliating butterfly Chlosyne sp. was collected from various localities within the distributional Rhodobaenus auctus Chevrolat range of T.diversifolia in Mexico, and was introduced (Coleoptera: Curculionidae) into quarantine in South Africa in 2007 and 2008. The stem-boring snout beetle R. auctus was Larvae of the butterfly are extremely damaging to collected on both T. rotundifolia and T. tubaeformis the leaves. Preliminary trials have shown that around the city of Cuarnavaca, Mexico, in 2007 oviposition and development occur on both inva- and 2008. The adult beetles are mainly black sive Tithonia species. Many of the larvae collected ventrally with a red dorsal thorax and elytra. As in in the field in 2007 and 2008 were heavily parasit- the case of C. mexicana, R. auctus has not been ized by various wasp species, and this limited the successfully reared under quarantine condi- number of adults available to start cultures and tions, but both species could be considered for to conduct host-specificity tests. This candidate further testing if the more damaging L. fimbrio- agent has thus been shelved. 448 African Entomology Vol. 19, No. 2, 2011
Fig. 5. Localities in Mexico where surveys for natural enemies of Tithonia species were undertaken during 2007 and 2008 in Mexico. ¢, Tithonia diversifolia; p, Tithonia rotundifolia.
An unidentified stem-boring moth (Lepidoptera: PATHOGENS OF THE TWO Tortricidae) TITHONIA SPECIES (Table 1) A very damaging, unidentified moth, was collected from T. diversifolia near Puerto Angel on Puccinia enceliae Dietel & Holw. the southeast coast of Mexico, and was introduced (Puccinales: Pucciniaceae) into South Africa in 2008 for host-specificity test- A number of destructive pathogens are known ing. Adults oviposit onto the shoot tips. The larvae to occur on T. diversifolia and T. rotundifolia in their burrow into the stems, feed internally, gradually native range (Farr & Rossman 2007), and these causing permanent wilting of the entire branch, were selected for further attention as potential and sometimes kill the whole plant. After preparing biological control agents. Isolates of one of the rust exit holes for adult emergence, larvae pupate within species, Puccinia enceliae, were collected from the stem. During multi-choice host-specificity T. diversifolia, T. rotundifolia and T. tubaeformis tests, the moth attacked several cultivars of sun- during 2007 and 2008 (Table 1), and were subse- flower Helianthus annuus L. (Asteraceae) and was quently introduced into the Agricultural Research therefore rejected. Council-Plant Protection Research Institute (ARC-PPRI) quarantine facility in Stellenbosch for Platyphora ligata (Stål) screening against the South African Tithonia (Coleoptera: Chrysomelidae) species. The spores from all the different isolates This leaf-feeding beetle was recorded on proved to be viable and were able to germinate T. diversifolia in Mexico during the present investi- and penetrate the cells on the leaf surface of the gations, and had been previously noted on this targeted South African Tithonia species. However, host plant in Costa Rica. Although it has never further investigation by light microscopy showed been imported into South Africa, nor studied fur- that there was no development beyond the point ther, it may have potential as a biological control of penetration. The reasons for this incompatibil- agent. ity between the rust isolates and the South African Simelane et al.: Biological control of Tithonia species (Asteraceae) 449 in T. diversifolia and T. rotundifolia biotypes remain unknown. Future studies on pathogens should include the
biotypes planting of trap-plants of South African biotypes of Tithonia species in Mexico to obtain compatible rust isolates, determination of possible influence
Tithonia diversifolia Tithonia of host-physiology on rust infection, and the expansion of surveys to previously unexplored and native regions (e.g. south east of Mexico, Guate- African mala and Costa Rica). A study on DNA matching of South African and Mexican populations of Tithonia species should also be considered during searches for compatible rust isolates.
Tithonia rotundifolia CONCLUSION
Although Tithonia species are primarily invaders of disturbed habitats, biological control could be a viable option for their management. The prospects for releasing biological control agents against T. rotundifolia appear promising. Efforts to find candidate agents for T. diversifolia, particularly the leaf-feeding beetle P. ligata which was previously recorded on this weed in Costa Rico, need to be intensified.
ACKNOWLEDGEMENTS October 2008October 2008 PuertoOctober Angel 2007 City, Mexico PuertoOctober Angel 2008 Mexico CuarnavacaOctober city, Mexico 2007 CentralOctober to 2008 South East of Cuarnavaca MexicoNot Mexico imported Host specificity in Puerto progress 2007, Angel 2008 City, Mexico Unsuccessfully reared From various locations Unsuccessfully in reared Host Mexico specificity tests initiated From various locations in Recorded Mexico in Costa Rica Not host specific, culled Host-specificity Incompatible with tests South shelved
Our special thanks go to A. Wood and S. Neser of
sp. Date imported Origin Status the ARC-PPRI for conducting field surveys and collecting natural enemies associated with weedy
rotundifolia October 2007 Mexico Citysunflowers Host specificity in progress in Mexico during 2007 and 2008, A.
Tithonia targeted T. diversifolia T. diversifolia T. rotundifolia Witt and anonymous reviewers for providing comments and suggestions on the manuscript, K. Malatji (ARC-PPRI) for providing technical assistance during the study, and to H. Brailovsky (Coleccion Nacional de Insectos, UNAM), E. Grobbelaar and S. Neser for facilitating the identi- fication of various insects associated with Tithonia sp. species. Financial support for this programme was provided by the Working for Water Programme of the South African Department of Water Affairs.
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