prospective agents for the biological control of … simelane et al...tithonia diversifolia (fig. 2)...

Prospective agents for the biological control of Tithonia rotundifolia (Mill.) S.F.Blakeand 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 Africa2Agricultural 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 andTithonia diversifolia (Hemsl.) A.Gray (Asteraceae: Heliantheae), were targeted for biologicalcontrol in South Africa. Surveys conducted in their native range (Mexico) revealed that therewere five potential biological control agents for T. rotundifolia, and three of these are currentlyundergoing host-specificity and performance evaluations in South Africa. Two leaf-feedingbeetles, 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-boringbeetle, Lixus fimbriolatus Boheman (Coleoptera: Curculionidae), is also highly damaging toT. 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 beconsidered for further testing if L. fimbriolatus is found to be unsuitable for release in SouthAfrica. Only two insect species were imported as candidate agents on T. diversifolia, theleaf-feeding butterfly Chlosyne sp. (Lepidoptera: Nymphalidae), and an unidentifiedstem-boring moth (Lepidoptera: Tortricidae): the latter was tested in quarantine but rejectedbecause it attacked several sunflower cultivars. Only one pathogen, Puccinia enceliae Dietel& Holw. (Uredinales: Pucciniaceae), was found that could potentially have been used as abiological control agent against the Tithonia species, but attempts to culture this rust wereunsuccessful.

Key words: red sunflower, Mexican sunflower, Zygogramma signatipennis, Zygogrammapiceicollis, Lixus fimbriolatus.

INTRODUCTION

Red sunflower, Tithonia rotundifolia (Mill.)S.F.Blake, and Mexican sunflower, Tithonia diversi-folia (Hemsl.) A.Gray (Asteraceae: Heliantheae),from Mexico have become invasive in the humidand sub-humid tropics of Central and SouthAmerica, South East Asia and tropical and sub-tropical Africa (Lazarides et al. 1997; Meyer 2000;Varnham 2006; Henderson 2001). The increasingabundance of T. rotundifolia and T. diversifolia inconservation and agricultural areas over the pastten years in South Africa has been of concern, re-sulting in the initiation of a biological controlprogramme against these two species in 2007.

The genus Tithonia comprises 11 species, withthe centre of distribution in Mexico, but with onespecies extending into the southwestern U.S.A.,and several species extending into some CentralAmerican countries (Muoghalu & Chuba 2005).

Tithonia rotundifolia (Fig. 1) is a large, robust annualplant and grows up to 3 m in height. The leaves ofT. rotundifolia are often paired, each triangular-ovate,or sometimes deeply three-lobed, and the red-dish-orange flowers are held singly on long stems.Tithonia diversifolia (Fig. 2) is a large evergreenperennial shrub and grows up to 5 m tall, and hasdeeply divided, paired leaves and orange-yellowflowers on erect, hollow woody stems. In SouthAfrica, flowering in T. rotundifolia occurs fromlate summer and throughout autumn, whileT. diversifolia flowers in autumn and winter.Tithonia rotundifolia produces fewer, larger andheavier seeds, which may explain its early andvigorous seedling growth and longer survival inrelatively unfavourable conditions (Muoghalu &Chuba 2005). By contrast, T. diversifolia producesnumerous, smaller, lighter seeds which allow fordispersal over large areas (Muoghalu & Chuba2005), and T. diversifolia cuttings, buried horizon-

African Entomology 19(2): 443–450 (2011)

*To whom correspondence should be addressed.E-mail: [email protected]

tally into the soil, often sprout, contributing to thedensification of stands of this species.

Deliberately introduced and widely cultivatedas ornamental plants, both T. rotundifolia andT. diversifolia have become invasive in the tropicsand subtropics (Lazarides et al. 1997; Meyer 2000),including several countries in sub-Saharan Africa(Chukwuka et al. 2007). In Nigeria, T. diversifolia isbecoming an important weed of arable crops inOyo, Gbongan and Ogun States, forcing somefarmers to abandon their lands (Chukwuka et al.2007). Following their introduction into SouthAfrica in the 1900s (Henderson 2006), both Tithoniaspecies are now invasive in KwaZulu-Natal(KZN), Limpopo and Mpumalanga provinces,with T. rotundifolia extending its range into theNorth West and Gauteng provinces (Fig. 3) andT. diversifolia being more abundant and wide-spread along the humid and low-altitude areasof Mpumalanga and KZN provinces (Fig. 4)

(Henderson 2001). Both T. rotundifolia and T. diver-sifolia are aggressive colonizers, particularly indisturbed, sun-exposed ecosystems, abandonedsites, and along railways and roads, and they aredeclared Category 1 weeds in South Africa(Henderson 2001).

Although the uses of Tithonia species as medicinalplants (Lin et al. 1993; Takahashi 1998; Tona et al.1998), livestock fodder (Roothaert & Paterson1997), poultry feed (Odunsi et al. 1996) and greenmanure (Nagarajah & Nizer 1982; Drechsel & Reck1998; Jama et al. 2000) are widely acknowledged invarious parts of the world, the problems theycause in Africa as invasive weeds far outweightheir benefits.

There are no herbicides registered for the controlof either of the Tithonia species in South Africa, andmechanical control is largely ineffective due to theability of T. diversifolia to coppice from stems andbecause of the rapid recruitment of seedlings of

444 African Entomology Vol. 19, No. 2, 2011

Fig. 1. Tithonia rotundifolia. (Drawn by W. Roux; first published in Henderson (1995), ARC-Plant Protection ResearchInstitute, Pretoria.)

X 1/2

X 3/4

X 3/4

100

mm

both species in cleared areas. Consequently, a bio-logical control programme was initiated, and fieldsurveys for potential biological control agentswere conducted in Mexico during 2007 and 2008(Fig. 5). Nine candidate agents were recorded onTithonia species at over 100 sites, and eight of thesewere subsequently introduced into quarantine inSouth Africa for further evaluation. The biology,host specificity and impact of those that wereintroduced and evaluated for possible release arereviewed below in descending order of their per-ceived suitability as biological control agents.

INSECT NATURAL ENEMIES OFTITHONIA ROTUNDIFOLIA

Zygogramma signatipennis (Stål) andZygogramma piceicollis (Stål)(Coleoptera: Chrysomelidae)

The two leaf-feeding beetles, Z. signatipennis andZ. piceicollis, are the most promising biologicalcontrol agents for T. rotundifolia. AlthoughZ. signatipennis was initially collected from aclosely-related plant species, Tithonia tubaeformis

(Jasq.) Cass, in and around Mexico City in 2007, itwas later recorded on T. rotundifolia at several sitesin the Oaxaca and Chiapas states of Mexico. In2008, Z. piceicollis was collected on T. rotundifolianear Puerto Angel, along the humid south coastregion of Mexico. Zygogramma signatipennis is thelarger of the two, and is shiny black in colour withsilver green markings on the elytra. Zygogrammapiceicollis has a dark red head and thorax with lightgrey markings on the elytra. The two beetle specieshave very similar life histories and feeding habits.Females of both species usually deposit their eggssingly on the lower leaf surface, mostly along theleaf veins, but occasionally on the flower heads.Adult and larval feeding by both beetle species onthe leaves is highly damaging, often skeletonizingthem completely. Late-instar larvae drop from thehost plant and burrow into the ground to pupate.Development from egg to adult takes about four tofive weeks.

To determine the host range of the two Zygo-gramma species, trials were initiated in 2008 underquarantine conditions in South African, and in thefield in Mexico. Preliminary results of paired- and

Simelane et al.: Biological control of Tithonia species (Asteraceae) 445

Fig. 2. Tithonia diversifolia. (Drawn by W. Roux; first published in Henderson (1995), ARC-Plant Protection ResearchInstitute, Pretoria.)

X 1/2

X 3/4

X 3/4

100

mm

no-choice tests indicated that both species ofZygogramma strongly prefer T. rotundifolia to otherclosely-related plant species for feeding, ovipositionand larval development. If, after further testing,they are found to be adequately host-specific toT. rotundifolia, permission to release both beetlespecies in South Africa will be sought. Surveys inMexico indicate that Z. signatipennis is predominantin drier inland regions while Z. piceicollis is mainlyfound in warm, humid coastal regions, whichmight indicate that the release of both speciescould result in effective control throughout thedistribution range of T. rotundifolia in South Africa.

Lixus fimbriolatus Boheman(Coleoptera: Curculionidae)

The stem-boring weevil L. fimbriolatus was col-lected from T. rotundifolia in Mexico and intro-duced into quarantine in South Africa in October2008. Lixus fimbriolatus adults, which are dark grey

to black in colour, are long-lived, with combinedpre-oviposition and oviposition periods of over12 months. The adults nibble along the margin ofthe leaf and lay their eggs into the stems, approxi-mately 4 cm above the soil surface. The larvae tun-nel in and hollow out the stem, which couldincrease the vulnerability of plants to wind dam-age. The larvae are very destructive, especiallywhen plants are attacked at an early stage of devel-opment. Larvae often pupate near the shoot tip,from where the adults emerge. Development fromthe egg to adult stage is completed in five to sixmonths. A reliable rearing technique has beendeveloped (Mawela & Simelane 2009), andhost-specificity studies on this weevil have beeninitiated.

Canidia mexicana Thomson(Coleoptera: Cerambycidae)

Larvae of the stem-boring longhorn beetle,


Fig. 3. Distribution of Tithonia rotundifolia in South Africa. (Drawn by L. Henderson; data source: SAPIA database,ARC-Plant Protection Research Institute, Pretoria.)

C. mexicana, were found almost everywherewithin the natural distribution of T. rotundifolia inMexico (Fig. 5). As in the case of L. fimbriolatus,C. mexicana adults deposit their eggs into the stem.Upon eclosion, the larvae tunnel in the stem,causing extensive damage. However, severalattempts to rear the beetle under quarantine labo-ratory conditions were unsuccessful.

Rhodobaenus auctus Chevrolat(Coleoptera: Curculionidae)

The stem-boring snout beetle R. auctus wascollected on both T. rotundifolia and T. tubaeformisaround the city of Cuarnavaca, Mexico, in 2007and 2008. The adult beetles are mainly blackventrally with a red dorsal thorax and elytra. As inthe case of C. mexicana, R. auctus has not beensuccessfully reared under quarantine condi-tions, but both species could be considered forfurther testing if the more damaging L. fimbrio-

latus proves to be unsuitable for release againstT. rotundifolia.

INSECT NATURAL ENEMIES OFTITHONIA DIVERSIFOLIA (Table 1)

Chlosyne sp. (Lepidoptera: Nymphalidae)A defoliating butterfly Chlosyne sp. was collected

from various localities within the distributionalrange of T. diversifolia in Mexico, and was introducedinto quarantine in South Africa in 2007 and 2008.Larvae of the butterfly are extremely damaging tothe leaves. Preliminary trials have shown thatoviposition and development occur on both inva-sive Tithonia species. Many of the larvae collectedin the field in 2007 and 2008 were heavily parasit-ized by various wasp species, and this limited thenumber of adults available to start cultures andto conduct host-specificity tests. This candidateagent has thus been shelved.


Fig. 4. Distribution of Tithonia diversifolia in South Africa. (Drawn by L. Henderson; data source: SAPIA database,ARC-Plant Protection Research Institute, Pretoria.)

An unidentified stem-boring moth (Lepidoptera:Tortricidae)

A very damaging, unidentified moth, wascollected from T. diversifolia near Puerto Angel onthe southeast coast of Mexico, and was introducedinto South Africa in 2008 for host-specificity test-ing. Adults oviposit onto the shoot tips. The larvaeburrow into the stems, feed internally, graduallycausing permanent wilting of the entire branch,and sometimes kill the whole plant. After preparingexit holes for adult emergence, larvae pupate withinthe stem. During multi-choice host-specificitytests, the moth attacked several cultivars of sun-flower Helianthus annuus L. (Asteraceae) and wastherefore rejected.

Platyphora ligata (Stål)(Coleoptera: Chrysomelidae)

This leaf-feeding beetle was recorded onT. diversifolia in Mexico during the present investi-gations, and had been previously noted on thishost plant in Costa Rica. Although it has neverbeen imported into South Africa, nor studied fur-ther, it may have potential as a biological controlagent.

PATHOGENS OF THE TWOTITHONIA SPECIES (Table 1)

Puccinia enceliae Dietel & Holw.(Puccinales: Pucciniaceae)

A number of destructive pathogens are knownto occur on T. diversifolia and T. rotundifolia in theirnative range (Farr & Rossman 2007), and thesewere selected for further attention as potentialbiological control agents. Isolates of one of the rustspecies, Puccinia enceliae, were collected fromT. diversifolia, T. rotundifolia and T. tubaeformisduring 2007 and 2008 (Table 1), and were subse-quently introduced into the Agricultural ResearchCouncil-Plant Protection Research Institute(ARC-PPRI) quarantine facility in Stellenbosch forscreening against the South African Tithoniaspecies. The spores from all the different isolatesproved to be viable and were able to germinateand penetrate the cells on the leaf surface of thetargeted South African Tithonia species. However,further investigation by light microscopy showedthat there was no development beyond the pointof penetration. The reasons for this incompatibil-ity between the rust isolates and the South African


Fig. 5. Localities in Mexico where surveys for natural enemies of Tithonia species were undertaken during 2007 and2008 in Mexico.�, Tithonia diversifolia; �, Tithonia rotundifolia.

T. diversifolia and T. rotundifolia biotypes remainunknown.

Future studies on pathogens should include theplanting of trap-plants of South African biotypesof Tithonia species in Mexico to obtain compatiblerust isolates, determination of possible influenceof host-physiology on rust infection, and theexpansion of surveys to previously unexplorednative regions (e.g. south east of Mexico, Guate-mala and Costa Rica). A study on DNA matchingof South African and Mexican populations ofTithonia species should also be considered duringsearches for compatible rust isolates.

CONCLUSION

Although Tithonia species are primarily invadersof disturbed habitats, biological control could be aviable option for their management. The prospectsfor releasing biological control agents against T.rotundifolia appear promising. Efforts to findcandidate agents for T. diversifolia, particularly theleaf-feeding beetle P. ligata which was previouslyrecorded on this weed in Costa Rico, need to beintensified.

ACKNOWLEDGEMENTS

Our special thanks go to A. Wood and S. Neser ofthe ARC-PPRI for conducting field surveys andcollecting natural enemies associated with weedysunflowers in Mexico during 2007 and 2008, A.Witt and anonymous reviewers for providingcomments and suggestions on the manuscript,K. Malatji (ARC-PPRI) for providing technicalassistance 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 Tithoniaspecies. Financial support for this programme wasprovided by the Working for Water Programme ofthe South African Department of Water Affairs.

REFERENCES

CHUKWUKA, K.S, OGUNYEMI, S. & FAWOLE, I. 2007.Ecological distribution of Tithonia diversifolia (Hemsl).A. Gray – A new exotic weed in Nigeria. Journal ofBiological Science 7: 709–719.

DRECHSEL, P. & RECK, B. 1998. Composted shrub-prunings and other organic manures for small-holder farming system in southern Rwanda. Agro-forestry Systems 39: 1–12.

FARR, D.F. & ROSSMAN, A.Y. 2007. Fungal Databases,Systematic Mycology and Microbiology Laboratory,


Tab

le1.

Nat

ural

enem

ies,

thei

rda

teof

impo

rtat

ion

(ifap

plic

able

),or

igin

and

stat

usre

leva

ntto

the

biol

ogic

alco

ntro

lofT

ithon

iaro

tund

ifolia

and

Tith

onia

dive

rsifo

liain

Sou

thA

fric

a.

Ord

erN

atur

alen

emy

Tith

onia

sp.

Dat

eim

port

edO

rigin

Sta

tus

targ

eted

Fam

ilyC

oleo

pter

a:C

hrys

omel

idae

Zyg

ogra

mm

asi

gnat

ipen

nis

T.ro

tund

ifolia

Oct

ober

2007

Mex

ico

City

Hos

tspe

cific

ityin

prog

ress

Col

eopt

era:

Chr

ysom

elid

aeZ

ygog

ram

ma

pice

icol

lisT.

rotu

ndifo

liaO

ctob

er20

08P

uert

oA

ngel

City

,Mex

ico

Hos

tspe

cific

ityin

prog

ress

Col

eopt

era:

Cur

culio

nida

eLi

xus

fimbr

iola

tus

T.ro

tund

ifolia

Oct

ober

2008

Pue

rto

Ang

elM

exic

oH

osts

peci

ficity

test

sin

itiat

edC

oleo

pter

a:C

urcu

lioni

dae

Rho

doba

enus

auct

usT.

rotu

ndifo

liaO

ctob

er20

07C

uarn

avac

aci

ty,M

exic

oU

nsuc

cess

fully

rear

edC

oleo

pter

a:C

eram

byci

dae

Can

idia

mex

ican

aT.

rotu

ndifo

liaO

ctob

er20

08C

entr

alto

Sou

thE

asto

fMex

ico

Uns

ucce

ssfu

llyre

ared

Lepi

dopt

era:

Nym

phal

idae

Chl

osyn

esp

.T.

dive

rsifo

liaO

ctob

er20

07C

uarn

avac

aM

exic

oH

ost-

spec

ifici

tyte

sts

shel

ved

Lepi

dopt

era:

Tort

ricid

aeU

nide

ntifi

edT.

dive

rsifo

liaO

ctob

er20

08P

uert

oA

ngel

City

,Mex

ico

Not

host

spec

ific,

culle

dC

oleo

pter

a:C

hrys

omel

idae

Pla

typh

ora

ligat

aT.

dive

rsifo

liaN

otim

port

edFr

omva

rious

loca

tions

inM

exic

oR

ecor

ded

inC

osta

Ric

aU

redi

nale

s:P

ucci

niac

eae

Puc

cini

atit

honi

aeT.

dive

rsifo

lia,

2007

,200

8Fr

omva

rious

loca

tions

inM

exic

oIn

com

patib

lew

ithS

outh

T.r

otun

difo

liaA

fric

anT

ithon

iabi

otyp

es

ARS, USDA. Online at: http://nt.ars-grin.gov/fungaldatabases/ (accessed November 2007).

HENDERSON, L. 1995. Plant Invaders of Southern Africa.Plant Protection Research Institute Handbook No. 5.Agricultural Research Council, Pretoria, South Africa.

HENDERSON, L. 2001. Alien Weeds and Invasive Plants: AComplete Guide to Declared Weeds and Invaders in SouthAfrica. Plant Protection Research Institute HandbookNo. 12. Agricultural Research Council, Pretoria,South Africa.

HENDERSON, L. 2006. Comparison of invasive plants inSouthern Africa originating from Southern temperate,Northern temperate and tropical regions. Bothalia 36:20–122.

JAMA, B., PALM, C.A., BURESH, R.J. & NIANG, A. 2000.Tithonia diversifolia as a green manure for fertilityimprovement in western Kenya: a review. AgroforestrySystems 49: 201–221.

LAZARIDES, M, COWLEY, K. & HOHNEN, P. 1997.CSIRO Handbook of Australian Weeds. CSIRO Pub-lishing. Collingwood, Victoria, Australia.

LIN, C.C., LIN, M.L. & LIN J.M. 1993. The anti-inflammatory and liver protective effect of Tithoniadiversifolia (Hemls.) A. Gray and Dicliptera chinensisJuss. extracts in rats. Phytotherapy Research 7: 305–309.

MAWELA, K.V. & SIMELANE, D.O. 2009. Hopesbrighten for biological control of weedy sunflowersin South Africa. Biocontrol News and Information 30:23–24.

MEYER, J.Y. 2000. Preliminary review of the invasiveplants in the Pacific Islands. Sherley, G. (Ed.) In: The

Invasive Species in the Pacific: A Technical Reviewand Draft Regional Strategy. 85–114. South PacificRegional Environment Programme (SPREP), Apia,Samoa.

MUOGHALU, J.I. & CHUBA, D.K. 2005. Seed germi-nation and reproductive strategies of Tithonia diver-sifolia (Hemsl.) Gray and Tithonia rotundifolia (P.M.)Blake. Applied Ecology and Environmental Research 3:39–46.

NAGARAJAH, S. & NIZER, B.M. 1982. Wild sunflower asa green manure for rice in the mid-country westzone. Tropical Agriculturist 138: 69–78.

ODUNSI, A.A., FARINU, G.O. & AKINOLA, J.O. 1996.Influence of dietary wild sunflower (Tithoniadiversifolia Hemsl. A. Gray) leaf meal on layers perfor-mance and egg quality. Nigerian Journal of AnimalProduction 23: 28–32.

ROOTHAERT, R. & PATTERSON, R.T. 1997. Recent workon the production and utilization of tree fodder inEast Africa. Animal Feed Science and Technology 69: 39–51.

TAKAHASHI, M. 1998. Composition for curing diabetesmellitus processes for the preparation of SAME, andusage of SAME. U.S. Patent Document, Patentnumber 5,773,004.

TONA, L., KAMBU, K. NGIMBI, N. CIMANGA, K. &VLIETINCK, A.J. 1998. Antiamoebic and phyto-chemical screening of some Congolese medicinalplants. Journal of Ethnopharmacology 61: 57–65.

VARNHAM, K. 2006. Non-native species in U.K. over-seas territories: a review. Joint Nature ConservationCommittee Report 372. Peterborough, U.K.


prospective agents for the biological control of … simelane et al...tithonia diversifolia (fig. 2)...

Documents