Prospective agents for the biological control of Tithonia rotundifolia

Prospective agents for the biological control of Tithonia rotundifolia (Mill.) S.F.Blake
and Tithonia diversifolia (Hemsl.) A.Gray (Asteraceae) in South Africa
1
1
2
D.O. Simelane *, K.V. Mawela & A. Fourie
1
2
Agricultural Research Council-Plant Protection Research Institute, Private Bag X134, Queenswood, 0121 South Africa
Agricultural 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: preliminary 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.)
S.F.Blake, and Mexican sunflower, Tithonia diversifolia (Hemsl.) A.Gray (Asteraceae: Heliantheae),
from Mexico have become invasive in the humid
and sub-humid tropics of Central and South
America, South East Asia and tropical and subtropical Africa (Lazarides et al. 1997; Meyer 2000;
Varnham 2006; Henderson 2001). The increasing
abundance of T. rotundifolia and T. diversifolia in
conservation and agricultural areas over the past
ten years in South Africa has been of concern, resulting in the initiation of a biological control
programme against these two species in 2007.
The genus Tithonia comprises 11 species, with
the centre of distribution in Mexico, but with one
species extending into the southwestern U.S.A.,
and several species extending into some Central
American countries (Muoghalu & Chuba 2005).
*To whom correspondence should be addressed.
E-mail: simelaned@arc.agric.za
Tithonia rotundifolia (Fig. 1) is a large, robust annual
plant and grows up to 3 m in height. The leaves of
T. rotundifolia are often paired, each triangular-ovate,
or sometimes deeply three-lobed, and the reddish-orange flowers are held singly on long stems.
Tithonia diversifolia (Fig. 2) is a large evergreen
perennial shrub and grows up to 5 m tall, and has
deeply divided, paired leaves and orange-yellow
flowers on erect, hollow woody stems. In South
Africa, flowering in T. rotundifolia occurs from
late summer and throughout autumn, while
T. diversifolia flowers in autumn and winter.
Tithonia rotundifolia produces fewer, larger and
heavier seeds, which may explain its early and
vigorous seedling growth and longer survival in
relatively unfavourable conditions (Muoghalu &
Chuba 2005). By contrast, T. diversifolia produces
numerous, smaller, lighter seeds which allow for
dispersal over large areas (Muoghalu & Chuba
2005), and T. diversifolia cuttings, buried horizonAfrican Entomology 19(2): 443–450 (2011)
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African Entomology Vol. 19, No. 2, 2011
X 3/4
100 mm
X 3/4
X 1/2
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
densification of stands of this species.
Deliberately introduced and widely cultivated
as ornamental plants, both T. rotundifolia and
T. diversifolia have become invasive in the tropics
and subtropics (Lazarides et al. 1997; Meyer 2000),
including several countries in sub-Saharan Africa
(Chukwuka et al. 2007). In Nigeria, T. diversifolia is
becoming an important weed of arable crops in
Oyo, Gbongan and Ogun States, forcing some
farmers to abandon their lands (Chukwuka et al.
2007). Following their introduction into South
Africa in the 1900s (Henderson 2006), both Tithonia
species are now invasive in KwaZulu-Natal
(KZN), Limpopo and Mpumalanga provinces,
with T. rotundifolia extending its range into the
North West and Gauteng provinces (Fig. 3) and
T. diversifolia being more abundant and widespread along the humid and low-altitude areas
of Mpumalanga and KZN provinces (Fig. 4)
(Henderson 2001). Both T. rotundifolia and T. diversifolia are aggressive colonizers, particularly in
disturbed, sun-exposed ecosystems, abandoned
sites, and along railways and roads, and they are
declared Category 1 weeds in South Africa
(Henderson 2001).
Although the uses of Tithonia species as medicinal
plants (Lin et al. 1993; Takahashi 1998; Tona et al.
1998), livestock fodder (Roothaert & Paterson
1997), poultry feed (Odunsi et al. 1996) and green
manure (Nagarajah & Nizer 1982; Drechsel & Reck
1998; Jama et al. 2000) are widely acknowledged in
various parts of the world, the problems they
cause in Africa as invasive weeds far outweigh
their benefits.
There are no herbicides registered for the control
of either of the Tithonia species in South Africa, and
mechanical control is largely ineffective due to the
ability of T. diversifolia to coppice from stems and
because of the rapid recruitment of seedlings of
Simelane et al.: Biological control of Tithonia species (Asteraceae)
445
X 3/4
100 mm
X 3/4
X 1/2
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 biological control programme was initiated, and field
surveys for potential biological control agents
were conducted in Mexico during 2007 and 2008
(Fig. 5). Nine candidate agents were recorded on
Tithonia species at over 100 sites, and eight of these
were subsequently introduced into quarantine in
South Africa for further evaluation. The biology,
host specificity and impact of those that were
introduced and evaluated for possible release are
reviewed below in descending order of their perceived suitability as biological control agents.
INSECT NATURAL ENEMIES OF
TITHONIA ROTUNDIFOLIA
Zygogramma signatipennis (Stål) and
Zygogramma piceicollis (Stål)
(Coleoptera: Chrysomelidae)
The two leaf-feeding beetles, Z. signatipennis and
Z. piceicollis, are the most promising biological
control agents for T. rotundifolia. Although
Z. signatipennis was initially collected from a
closely-related plant species, Tithonia tubaeformis
(Jasq.) Cass, in and around Mexico City in 2007, it
was later recorded on T. rotundifolia at several sites
in the Oaxaca and Chiapas states of Mexico. In
2008, Z. piceicollis was collected on T. rotundifolia
near Puerto Angel, along the humid south coast
region of Mexico. Zygogramma signatipennis is the
larger of the two, and is shiny black in colour with
silver green markings on the elytra. Zygogramma
piceicollis has a dark red head and thorax with light
grey markings on the elytra. The two beetle species
have very similar life histories and feeding habits.
Females of both species usually deposit their eggs
singly on the lower leaf surface, mostly along the
leaf veins, but occasionally on the flower heads.
Adult and larval feeding by both beetle species on
the leaves is highly damaging, often skeletonizing
them completely. Late-instar larvae drop from the
host plant and burrow into the ground to pupate.
Development from egg to adult takes about four to
five weeks.
To determine the host range of the two Zygogramma species, trials were initiated in 2008 under
quarantine conditions in South African, and in the
field in Mexico. Preliminary results of paired- and
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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
Zygogramma strongly prefer T. rotundifolia to other
closely-related plant species for feeding, oviposition
and larval development. If, after further testing,
they are found to be adequately host-specific to
T. rotundifolia, permission to release both beetle
species in South Africa will be sought. Surveys in
Mexico indicate that Z. signatipennis is predominant
in drier inland regions while Z. piceicollis is mainly
found in warm, humid coastal regions, which
might indicate that the release of both species
could result in effective control throughout the
distribution range of T. rotundifolia in South Africa.
Lixus fimbriolatus Boheman
(Coleoptera: Curculionidae)
The stem-boring weevil L. fimbriolatus was collected from T. rotundifolia in Mexico and introduced into quarantine in South Africa in October
2008. Lixus fimbriolatus adults, which are dark grey
to black in colour, are long-lived, with combined
pre-oviposition and oviposition periods of over
12 months. The adults nibble along the margin of
the leaf and lay their eggs into the stems, approximately 4 cm above the soil surface. The larvae tunnel in and hollow out the stem, which could
increase the vulnerability of plants to wind damage. The larvae are very destructive, especially
when plants are attacked at an early stage of development. Larvae often pupate near the shoot tip,
from where the adults emerge. Development from
the egg to adult stage is completed in five to six
months. A reliable rearing technique has been
developed (Mawela & Simelane 2009), and
host-specificity studies on this weevil have been
initiated.
Canidia mexicana Thomson
(Coleoptera: Cerambycidae)
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
within the natural distribution of T. rotundifolia in
Mexico (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, several
attempts to rear the beetle under quarantine laboratory conditions were unsuccessful.
Rhodobaenus auctus Chevrolat
(Coleoptera: Curculionidae)
The stem-boring snout beetle R. auctus was
collected on both T. rotundifolia and T. tubaeformis
around the city of Cuarnavaca, Mexico, in 2007
and 2008. The adult beetles are mainly black
ventrally with a red dorsal thorax and elytra. As in
the case of C. mexicana, R. auctus has not been
successfully reared under quarantine conditions, but both species could be considered for
further testing if the more damaging L. fimbrio-
latus proves to be unsuitable for release against
T. rotundifolia.
INSECT NATURAL ENEMIES OF
TITHONIA DIVERSIFOLIA (Table 1)
Chlosyne sp. (Lepidoptera: Nymphalidae)
A defoliating butterfly Chlosyne sp. was collected
from various localities within the distributional
range of T. diversifolia in Mexico, and was introduced
into quarantine in South Africa in 2007 and 2008.
Larvae of the butterfly are extremely damaging to
the leaves. Preliminary trials have shown that
oviposition and development occur on both invasive Tithonia species. Many of the larvae collected
in the field in 2007 and 2008 were heavily parasitized by various wasp species, and this limited the
number of adults available to start cultures and
to conduct host-specificity tests. This candidate
agent has thus been shelved.
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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:
Tortricidae)
A very damaging, unidentified moth, was
collected from T. diversifolia near Puerto Angel on
the southeast coast of Mexico, and was introduced
into South Africa in 2008 for host-specificity testing. Adults oviposit onto the shoot tips. The larvae
burrow into the stems, feed internally, gradually
causing permanent wilting of the entire branch,
and sometimes kill the whole plant. After preparing
exit holes for adult emergence, larvae pupate within
the stem. During multi-choice host-specificity
tests, the moth attacked several cultivars of sunflower Helianthus annuus L. (Asteraceae) and was
therefore rejected.
Platyphora ligata (Stål)
(Coleoptera: Chrysomelidae)
This leaf-feeding beetle was recorded on
T. diversifolia in Mexico during the present investigations, and had been previously noted on this
host plant in Costa Rica. Although it has never
been imported into South Africa, nor studied further, it may have potential as a biological control
agent.
PATHOGENS OF THE TWO
TITHONIA SPECIES (Table 1)
Puccinia enceliae Dietel & Holw.
(Puccinales: Pucciniaceae)
A number of destructive pathogens are known
to occur on T. diversifolia and T. rotundifolia in their
native range (Farr & Rossman 2007), and these
were selected for further attention as potential
biological control agents. Isolates of one of the rust
species, Puccinia enceliae, were collected from
T. diversifolia, T. rotundifolia and T. tubaeformis
during 2007 and 2008 (Table 1), and were subsequently introduced into the Agricultural Research
Council-Plant Protection Research Institute
(ARC-PPRI) quarantine facility in Stellenbosch for
screening against the South African Tithonia
species. The spores from all the different isolates
proved to be viable and were able to germinate
and penetrate the cells on the leaf surface of the
targeted South African Tithonia species. However,
further investigation by light microscopy showed
that there was no development beyond the point
of penetration. The reasons for this incompatibility between the rust isolates and the South African
Host specificity in progress
Host specificity in progress
Host specificity tests initiated
Unsuccessfully reared
Unsuccessfully reared
Host-specificity tests shelved
Not host specific, culled
Recorded in Costa Rica
Incompatible with South
African Tithonia biotypes
Mexico City
Puerto Angel City, Mexico
Puerto Angel Mexico
Cuarnavaca city, Mexico
Central to South East of Mexico
Cuarnavaca Mexico
Puerto Angel City, Mexico
From various locations in Mexico
From various locations in Mexico
October 2007
October 2008
October 2008
October 2007
October 2008
October 2007
October 2008
Not imported
2007, 2008
T. rotundifolia
T. rotundifolia
T. rotundifolia
T. rotundifolia
T. rotundifolia
T. diversifolia
T. diversifolia
T. diversifolia
T. diversifolia,
T. rotundifolia
Family
Coleoptera: Chrysomelidae
Coleoptera: Chrysomelidae
Coleoptera: Curculionidae
Coleoptera: Curculionidae
Coleoptera: Cerambycidae
Lepidoptera: Nymphalidae
Lepidoptera: Tortricidae
Coleoptera: Chrysomelidae
Uredinales: Pucciniaceae
Zygogramma signatipennis
Zygogramma piceicollis
Lixus fimbriolatus
Rhodobaenus auctus
Canidia mexicana
Chlosyne sp.
Unidentified
Platyphora ligata
Puccinia tithoniae
Status
Origin
Date imported
Tithonia sp.
targeted
Natural enemy
Order
Table 1. Natural enemies, their date of importation (if applicable), origin and status relevant to the biological control of Tithonia rotundifolia and Tithonia diversifolia in
South Africa.
Simelane et al.: Biological control of Tithonia species (Asteraceae)
449
T. diversifolia and T. rotundifolia biotypes remain
unknown.
Future studies on pathogens should include the
planting of trap-plants of South African biotypes
of Tithonia species in Mexico to obtain compatible
rust isolates, determination of possible influence
of host-physiology on rust infection, and the
expansion of surveys to previously unexplored
native regions (e.g. south east of Mexico, Guatemala 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.
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
Our special thanks go to A. Wood and S. Neser of
the ARC-PPRI for conducting field surveys and
collecting natural enemies associated with weedy
sunflowers in Mexico during 2007 and 2008, A.
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 identification of various insects associated with Tithonia
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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