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Strawberry Guava (Psidium cattleianum) Prospects for Biological Control

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The impacts of seven species of insects that have significant deleterious effects on Psidium cattleianum (Strawberry guava) are presented. A leaf gall produced by Tectococcus ovatus (Homoptera, Eriococcidae) is the most promising potential agent due to the damage caused and its ease of handling. Bud galls forrned in response to Dasineura gigantea (Diptera, Cecidomyiidae) are precocious developments of the bud that terrninate shoot growth. A shoot gall produced by Eurytoma sp. (Hymenoptera, Eurytomidae) terminates further growth of the shool. A seed gall induced by Eurytoma sp. (Hymenoptera, Eurytomidae) cements groups of seeds together and prevents germination of all seeds in the fruit. Another leaf gall forrned in response to an unknown species of Psyllidae though species specific has little impact on the plants. The sawfly, Haplostegus epimelas (Hymenoptera, Pergidae) is unsuitable for biologica1 control because it attacks commercial guava occasionally. The chrysomelid Lamprosoma azureum (Coleoptera, Chrysomelidae) is not recommended because it attacks a number of myrtaceous species.
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Content Preview
Proceedings of the X International Symposium on Biological Control of Weeds 4-14 July 1999, Montana
State University, Bozeman, Montana, USA Neal R. Spencer [ed.]. pp. 659-665 (2000)
Strawberry Guava (Psidium cattleianum) Prospects
for Biological Control

C. WIKLER(1), J. H, PEDROSA-MACED0(2), M. D.
VITORIN0(3), M. G. CAXAMBÚ(2), and C. W. SMITH(4)
IDECIE - UNICENTRO - Universidade do Centro-Oeste, PR 153 - KM 7 - Bairro
Riozinho - C. Posta121, 84500-000 - Irati - PR - Brazil
2 Federal University of Parana, Laboratory of Forest Protection, Fax: 55 41 253-
2332, Av. Pref. Lothário Meissner, 3400 - Botanic Garden 80210-170 - Curitiba -
PR - Brazi1 3Av. República Argentina, 2534 Apto 14-A, Bairro Portão, Curitiba-
PR, Brasil, CEP: 80610-260 4 Department of Botany, University of Hawaii at
Manoa, 3190 Maile Way, Hono1ulu Hawaii 96822, USA

Abstract
The impacts of seven species of insects that have significant deleterious effects on
Psidium cattleianum (Strawberry guava) are presented. A leaf gall produced by
Tectococcus ovatus (Homoptera, Eriococcidae) is the most promising potential agent
due to the damage caused and its ease of handling. Bud galls forrned in response to
Dasineura gigantea (Diptera, Cecidomyiidae) are precocious developments of the bud
that terrninate shoot growth. A shoot gall produced by Eurytoma sp. (Hymenoptera,
Eurytomidae) terminates further growth of the shool. A seed gall induced by
Eurytoma sp. (Hymenoptera, Eurytomidae) cements groups of seeds together and
prevents germination of all seeds in the fruit. Another leaf gall forrned in response to
an unknown species of Psyllidae though species specific has little impact on the
plants. The sawfly, Haplostegus epimelas (Hymenoptera, Pergidae) is unsuitable for
biologica1 control because it attacks commercial guava occasionally. The
chrysomelid Lamprosoma azureum (Coleoptera, Chrysomelidae) is not recommended
because it attacks a number of myrtaceous species.
Introduction
Psidium cattleianum Sabine (Myrtaceae) known as araçá in Brazil and strawberry
guava in many other parts of the world was introduced in Hawaii about 1825. It is the
highest priority weed for contro1 in forests. Conventional mechanical and chemical
control methods are only feasible in small areas leaving an enormous pool of trees to
reinfest conserved areas and do not reach the seed bank in the soil. The potential for
biological control was considered to be low because any agent must have a significant
impact on P. cattleianum but not the closely related, commercially important P.
guajava.

Early exploratory work was not encouraging. In March 1991 the U.S. National
Park Service through its cooperative program at the University of Hawaii at Manoa
entered into an agreement with the Paraná Forestry Foundation (FUPEF), Federal
University of Paraná, Brazil, to study the insects that attacked P. cattleianum in
subtropical Brazil. It had earlier been decided that there were no pathogens that were
suitable. This paper presents a summary of the insects for consideration for use as
biological control agents plus two that were initially promising but later found to
attack P. guajava. They might be used as control agents in areas where guava is not an
important crop but only under certain very special circumstances.

Material and Methods
Psidium cattleianum is distributed in the Atlantic Forest of Brazil from Espirito
Santo south to northern Uruguay. Ali of the research presented in this paper was
conducted in the State of Paraná, Brazil, the center of the range. Exploratory research
was conducted from the coastal restinga to the First Plateau of Paraná State but the
detailed ecological studies were restricted to areas of the First Plateau (Balsa Nova,
Centro Poli técnico, Estância Bethânia, Guaraguaçú, Juruqui, Mananciais da Serra,
Taboão, Nursery of the Forestry Course and São Femando Farm). The laboratory and
garden experiments were conducted at the Forest Protection Laboratory, Federal
University of Paraná, Curitiba.


Results
POTENTIAL BIOLOGICAL CONTROL AGENTS. BUD GALL - Dasineura
gigantea
(Diptera, Cecidomyiidae)
The bud galls form small rosettes up to 3 cm diameter somewhat like a double
flower due to precocious production and development of the leaves that probably
outpaces the ability of the meristem to produce embryonic tis sue. The rosettes are
initially green but then turn yellow as they age and finally turn a deep purple before
drying out and turning brown. The arrangement of the leaves in the rosette is irregular
on a very compressed shoot in contrast to another recently discovered bud gall in
which the leaves are regularly arranged around a short stem up to 1.5 cm long. The
galls can be found on trees throughout the range of the weed. It attacks both the red
and yellow-fruited forms (Angelo, 1997).

Brief Description of Insect
Two parasitoids that attack D. gigantea are known. Leptacis sp. (Hymenoptera,
Platygasteridae) is very small (1,5-2,0 mm) with previous wings reaching of length.
The geniculated antennae is inserted in the inferior portion of the head with 10 articles
(males with the fourth specialized segment), gaster moderately chitinous, with six or
less visible tergites and the ovipositor hidden at resto This parasitoid is found
throughout the range of D. gigantea. The other parasitoid is an unidentified species in
the Braconidae, Alysiinae. It is small yellow-orange being winged with previous
wings reaching of 3 to 5 length mm. There are more than 16 segments in the antennae,
which are not geniculated and not club. The jaws are exodonts with 3-7 teeth, gaster
with tergites 2 and 3 usually melted.
The insect forms galls in terminal and lateral buds of flush shoots occasionally
producing diminutive galls in flowers and more rarely fruits. The production of the
gall ceases the activity of the apical meristem of the affected shoot killing it. Heavily
infested shoots do not grow any further. Any future activity of that branch results
from the growth of a lower bud released from the apical dominance of the terminal
parts.
This agent is a very promising agent because it will not kill the trees. The death of
a large number of trees in monotypic stands, as in Hawaii, is a concern of forest
managers due to the increased potential for erosion. How effective this insect will be
when exposed to species of braconid and platygasterid parasitoids which are less
species specific is not known. The wide ecological range of the species makes it a
generally useful agent. There is a potential cultural use of the galls in Hawaii where
they could be substituted for green roses which are frequently used in leis.

Lamprosoma azureum (Coleoptera, Chrysomelidae)
Both the larvae and adults damage the plants by feeding on the young,
unsc1erified bark of the shoots frequently girdling it. Even if the girdling is incomplete
the shoot is severely stunted and very susceptible to attack by pathogens. The beetles
attack young trees only and have never been observed on plants above 1.8-m height.
The highest number of insects on one plant was 8 where they cause extensive damage.

This chrysomelid is confined to the upper elevations of the distribution of the boost
plant above 650 m.
The adult is a brilliant metallic blue beetle with a flat body approximately 4 mm in
length. The larvae in their scatoshell are usually found in the axils of branches but are
also found occasionally on young branches.

Natural enemies inc1ude some unidentified Hymenoptera. They attack the larvae in
the scatoshell.
The activity of the beetles and their larvae stresses the strawberry guava plants
considerably. Chrysomelids are generally favoured in biological control because of the
damage they cause and their specificity (Julien, 1993). Unfortunately, this species is
not specific to strawberry guava. It has been found feeding on the following species of
Myrtaceae: Eugenia uniflora L., Campomanesia xanthocarpa Berg, Psidium guajava
L., P. spathulatum Mattos and Acca sellowiana Berg. The scatoshell were also
observed on two species of Melastomataceae: Tibouchina sellowiana (Cham.)
Cogniaux and Tibouchina urvilleana (De.) Cogniaux. This is thought to be the first
record of a chrysomelid beetle on Melastomataceae (Caxambú, 1998).


LEAF GALL (Hemiptera, Psyllidae)
The insect produces large, round green galls on the leaves. The insect is found
throughout the range of P. cattleianum. Emergency of the psyllids occurs from
October to November and they copulate 5-10 minutes after the emergency. The
posture occurs mainly in the margin of the limbo, with the eggs attached in the
pedicel. The adults live around 5 days and feed the sap in the leaves. The nymphs
hatch and after short displacement they fix in the in the adaxial surface and start
feeding.
After intense hiperplasy, these cells hypertrofy and start the gall formation with
growth and projection in the inferior part of the leaf. The gall has round shape with 5
mm diameter in average. The amount of galls are variable, sometimes more than 70
by leaf. The nymphs can have 4-5 ecdysis inside the gall and become adults inside of
the gall. The gall tissues only break up with the adults formation when they are
released to the exterior.

The adults are predated by wasps, ants, flies, spiders and birds. The nymphs are
protected inside the galls but also can be attacked by parasitoids.
This species, though apparently confined to P. cattleianum, will probably not be an
effective biological control agent. The damage that it causes does not result in
premature leaf drop or any reduction in flowering or growth of the plants.

LEAF GALL - Tectococcus ovatus (Homoptera, Eriococcidae)
The gall is convex oval on one side of the leaf, and acuminate oval on the other.
The acuminate portion is generally on the upper side of the leaf whether or not that is
the abaxial surface. Occasionally galls may have acuminate or convex forms on both
sides of the leaf. The size of the galls is very variable, depending on the developmental
stage and the sex of the insect, those containing adult males are narrower and more
acuminate than females. The maximum diameter of the gall varies from 0,95 - 7.9 mm
on the acuminate side and 1,55-7,0 mm on the convex side. The depth of the galls
from the acuminate tip to the top of the convex portion varied from 1,80-8,5 mm. The
galls are the same colour as the leaf though the tips are frequently red (Vitorino,
1998).
Tectococcus ovatus is distributed throughout the range of P. cattleianum in Brazil
but it much more frequent on the red-fruited form on the First Plateau.
The adult female is oval (1,1-3,7 by 0.8-2.0 mm), translucent rosy-white, turgid,
fragile, and wingless with black eyes. The legs are legs but apparently do not function.
The anal ring is hairless. The rostrum is small in comparison to the body. The length
of the insects is varied. The males are smaller, yellow-gold with a pair of wings, long
legs, and an atrophied buccal apparatus.
There is one parasitoid, Metaphycus flavus (Hymenoptera, Encyrtidae). The
percentage parasitism in Brazil is 49%. There is also an ectoparasite Aprostocetus sp.
Westwood, 1883 (Hymenoptera, Eulophidae) but the percentage parasitism is only 1
%. There is also a predator, Hyperaspis de/icata Massuti and Vitorino (Coleoptera,
Coccinellidae) (Almeida & Vitorino, 1997). The percentage parasitism of galls is 5%.
SAWFLY - Haplostegus epimelas (Hymenoptera, Pergidae)
The sawfly can cause extensive damage to young shoots and mature leaves of P.
cattleianum. The eggs are laid subepidermally along the length of one si de of the
shoot which slows the growth of that side considerably. Further damage and fungal
growth can result in death of the twig. The young nymphs feed on the undersurface of
the leaves which in conjunction with oviposition kills a larger percentage of shoots.
The later instars consume large quantities of the mature leaves defoliating shoots
(Pedrosa-Macedo, 1998). The sawflies can be found throughout the range of P.
cattleianum.

The caterpillars are the most obvious phase of the life cycle of this insect and the
one that creates the damage of the plants. It is yellowish to occasionally. There are no
spots along the body though the dark intestine is visible. The mature caterpillars are
about 2 cm longo The aggregated caterpillars feed voraciously on the leaves stripping
them within one or two hours.
The eggs are damaged by a species of mites which suck out the contents of the
eggs. There is a Pentatomid that attacks the larvae. The percentage parasitismm by
these predators is less than 1 %. A Vibrissina sp. (Diptera: Tachinidae) parasitoid
results in the death of 4% of the insects. The greatest loss in populations (up to 50%)

are in the prepupal and pupal stages in the soil where they are susceptible to fungal
diseases.
The potential of the sawfly as a biological control agent is poor. Previous reports
had indicated that the sawfly also attacks P. guajava but during 4 years study we have
had only 2 observations out of a minimum of over 300 comparative studies. The
sawfly obviously has a high .preference for P. cattleianum. The low number of events
where the sawfly attacks P. guajava may indicate that only certain varieties or
perhaps plants weakened by other factors are attacked. The problem needs further
study because we have not yet confirmed that the sawfly completes its life cycle on
this plant.
SEED GALL - Sycophila sp. (Hymenoptera, Eurytomidae)
The insect lays its eggs in young buds and open flowers up until pollination but not
those where the floral organs are beginning to deteriorate. Fruit containing seed galls
have a lumpy, deformed appearance and are generally larger than the smooth. normal
fruit. The seeds are cemented together in large masses or a few smaller masses and
contain considerably less pulp than in normal fruit. Apparently normal seeds may be
found in the galls but they and the seed masses fail to germinate (Wikler, 1999;
Wikler, this volume).
The insect is found throughout the range of Psidium cattleianum. It does not
demonstrate any preference for any type of fruit or ecological situation. It was also
found in Psidium longipetiolatum, plant that according to Klein (1990) is a mutation
originated from P. cattleianum, which is intimateiy connected by the
macromorphologic aspects, but it is a much larger tree.
The adult female is yellowish to light brown with a large black stripe from the
middle of the pronotum to the posterior end. The males are predominantly black.
There is a small carina running down the whole length of the gena. Males and females
can be readily distinguished from one another not only by the presence/absence of the
ovipositor. The female is larger, predominantly brownish yellow pale In the abdomen
the stripe has triangular lateral branches.
There is one natural enemy, the parasitoid Torymus sp. (Hymenoptera,
Torymidae). These insects are readily distinguishable from the gall former by their
generallight brown with a striking metallic green mesosoma, metasoma, and half of
the posterior coxa. The females have a very long ovipositor with which they lay their
eggs in young fruit including those showing early signs of deformation due to the
activity of the gall former.
Fruit with gall fall to the ground at the same time as normal fruit. None of the
seeds in galled fruit germinate. Galls can be found in the leaf litter of trees for at least
two years after fruit drop. Laboratory studies showed that the bulk of the insects
emerge from 4-10 weeks later but the presence of live larvae in the galls.
The prospects of this insect as a biological control agent are high. It will be
difficult but not necessarily impossible to coordinate the emergence of insects with
floral bud production in some areas. The ability of this insect to attack plants
throughout its range is a considerable advantage. An insect that reduces seed viability,
however, is a long-term control agent that may not be suitable for managers looking
for more immediate reductions in population levels of the weed. It will, however, have
a strong effect in controlling dissemination of the weed in areas where range
expansion is still occurring. There is a potential conflict of interest with
horticulturalists who grow the plant for its fruit. Galled fruit are somewhat unsightful
and the rough texture of the seed masses somewhat unpalatable.

STEM GALL - Eurytoma sp. (Hymenoptera, Eurytomidae)
The stem galls are predominantly lightly dilated to round, 2-3 times the diameter
of the stem at the base of a short shoot. The gall is the same colour as the stem,
initially green but slowly turning brown with age. The size of the galls varied from
0.6-2.1 cm long by 0.3-0.9 cm wide (Wikler, 1995; Wikler et aI., 1996).
The species is confined to the First Plateau (800-1100m). The adult insects are
black in both sexes. The main characteristics are the roughly punctate thorax and the
large, square pronotum which when seen from above is as wide as the mesonotum.
There are no known natural enemies while the insect is inside the gall. After emer-
gence, it is attacked by several insects and birds.
The insect attacks emerging shoots, the gall developing at the base of the shoot
which is generally somewhat stunted. Leaf development is normal but no flower buds
are formed as on uninfested adjacent shoots. At the end of the growing season the

shoot distal to the gall dies terminating growth of that branch. Heavily infested plants,
therefore, are somewhat stunted when compared with adjacent uninfested plants.
The insect appears to be species specific attacking both the yellow and red-fruited
forms but shows a marked preference for the red-fruited form. It does not attack the
commercial guava or other representative myrtaceous species. Nor does it attack
common species adjacent to plants in native forests, e.g., Baccharis spp. (Asteraceae),
Rapanea ferruginea (Myrsinaceae), Schinus terebinthifolius (Anacardiaceae),
Tibouchina spp. (Melastomataceae), Vernonia spp. (Asteraceae). Its restricted
occurrence to the higher elevations of the distribution of P. cattleianum means that it
has limited potential as a universal agent against this plant. Hawaiian forest managers,
however, are interested because the critical areas for conservation of Hawaiian native
forests are all at higher elevations where potential conflicts of interest with fruit
fanciers and horticulturists are minimal.

Acknowledgments
Sincere thanks are due to Drs. Vinalto Graf, Luís of Santis, John La SalIe, Dr.
Donald J. Quicke, Dr. Lúcia Massuti de Almeida, Dr. Ayres Menezes, MSc. Maria
Christina Almeida, Dr. Jocélia Orazia and Dr. Csaba Thuroczy for considerable
assistance with their attempts to identify the species found in this study. This study
was supported in part by funding from CNPq, Brazil, V.S. National Park Service and
the University of Hawaii (CA80xx-2-9004). Many thanks to Letícia Penno de Sousa,
Alessandro Camargo Ângelo, Nilton José Sousa, and César Assis Butignol from the
Laboratory of Forest Protection, for their excellent assistance.

References
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