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Bustillo et al.: B. bassiana and M. anisopliae


DYNAMICS OF BEAUVERIA BASSIANA AND METARHIZIUM
ANISOPLIAE INFECTING HYPOTHENEMUS HAMPEI
(COLEOPTERA: SCOLYTIDAE) POPULATIONS EMERGING
FROM FALLEN COFFEE BERRIES

ALEX E. BUSTILLO1, MARTHA G. BERNAL PABLO BENAVIDES' AND BERNARDO CHAVES2
1Disciplina de Entomologia, 2Disciplina de Biometria, Centro Nacional
de Investigaciones de Caf6, Cenicaf6, Chinchind, Caldas, Colombia

ABSTRACT

The aim of this research was to evaluate the effect of soil sprays of the ento-
mopathogens Beauveria bassiana and Metarhizium anisopliae on coffee berry borer
(cbb) adults, Hypothenemus hampei, emerging from fallen berries through time. Each
fungus was applied to a plot 5000 m2 in size of the Colombian variety in the third har-
vest year. The experimental plot was formed with 9 trees, and the experimental unit
was the central tree. In this tree all the green uninfested berries were left and the
whole tree covered with a screen cage to avoid further cbb infestation or escape. Nine
treatments replicated ten times were arranged in a complete randomized design.
Conidia of each fungus were suspended in emulsified oil and water and applied on the
base of the trees at a dosage of 1 x 109 conidia/tree. Under each experimental tree 350
cbb-infested coffee berries were placed on the soil to serve as a source for aerial infes-
tation of the trees. Infested berries were applied the same day of the spray and at 2,
5, 10, 15, 20, 25 and 30 days after fungus application. Results showed that infection
levels of both fungi on cbb were the highest during the first five days after application,
reaching nearly 30% for B. bassiana and 11% for M. anisopliae. However, the infection
decreased for 20 days but peaked again at 25 days post-treatment with 24.3% for
B. bassiana and 7.7% for M. anisopliae. These results are explained by the formation
of propagules in the soil by these fungi, due probably to the accumulation of infective
conidia on infected insects which infect other insects leaving the fruits. The two spe-
cies were recovered from the soil even after two months and fluctuation in numbers
of colony forming units was attributed to the rainfall during the study period and the
fungus conidiation. B. bassiana was shown to be more infective than M. anisopliae,
considering that the latter is more frequently associated to soil habitats. The authors
believe efficiency of these fungi can be increased if improvements are made to the for-
mulations, e.g., using a granulated formulation to avoid leaching of the conidia from
the soil during heavy rainy seasons. During this study it was found that H. hampei is
a new host of Paecilomyces lilacinus.

Key Words: Coffee berry borer, Hypothenemus hampei, Beauveria bassiana, Metarhi-
zium anisopliae, Paecilomyces lilacinus

RESUME

Este studio evalu6 el efecto de aspersiones de Beauveria bassiana y Metarhizium
anisopliae al suelo sobre la broca del caf6, Hypothenemus hampei, que emerge de fru-
tos caidos, a media que transcurre el tiempo despues de depositar el hongo. Se selec-
cionaron dos lotes de caf6 variedad Colombia de tercera cosecha con un area de 5000
m2 y se evaluaron los dos hongos en lotes experimentales diferentes. La parcela se
form con 9 arboles y el arbol central se escogi6 como la unidad experimental. A este
arbol se le dej6 solo frutos verdes sin infestaci6n por broca y se cubri6 con una jaula
entomol6gica para evitar nuevas infestaciones o escape de broca. Las conidias de los
hongos utilizados se suspendieron en aceite emulsionable y agua usando una dosis de
1 x 109 conidias/arbol. En la base del arbol que sirvi6 como unidad experimental se as-

















Florida Entomologist 82(4)


December, 1999


perjaron los hongos al plato de cada arbol y se depositaron 350 frutos brocados el
mismo dia de la aspersi6n y 2, 5, 10, 15, 20, 25 y 30 dias despu6s de la aspersi6n. Los
resultados muestran niveles maximos de infecci6n durante los cinco primeros dias
posterior a la aspersi6n de los hongos, cercanos al 30% para B. bassiana y 11% para
M. anisopliae. Sin embargo la infecci6n disminuy6 y de nuevo alcanz6 un nuevo pico
hacia el dia 25 de la evaluaci6n. Despu6s de este tiempo la infecci6n se increments
nuevamente hasta niveles similares a los alcanzados en los 5 primeros dias, 24,3% y
7,7% para B. bassiana y M. anisopliae respectivamente. Estos resultados se pueden
explicar por la formaci6n de propagulos en el suelo por estos hongos, debido probable-
mente a la acumulaci6n de conidias infectivas sobre insects atacados que infectan
otros insects que salen de los frutos. Las dos species se recuperaron del suelo aun
despu6s de dos meses y la fluctuaci6n en el numero de las unidades formadoras de co-
lonia se atribuy6 a la precipitaci6n y a la conidiaci6n del hongo. B. bassiana mostr6 un
efecto superior al de M. anisopliae, si se tiene en cuenta que este ultimo esta mas aso-
ciado a condiciones del suelo. La eficiencia de estos hongos se podria mejorar con for-
mulaciones granuladas del hongo que permitan una mayor permanencia en el suelo
para disminuir la lixiviaci6n causada por las lluvias. Durante el studio se constat6
que H. hampei es un nuevo hu6sped de Paecilomyces lilacinus.





The coffee berry borer (cbb), Hypothenemus hampei (Ferrari), was introduced into
Colombia in 1988 and now is widespread in the major coffee producing area where it
is the most important insect pest (Bustillo 1991). Infested coffee berries that fall to
the soil are the main source of reinfestation of the coffee plantations at the end of the
harvest period. Traditionally, the berries that fall during the harvest period are not
harvested because this practice is very tedious and expensive. In Colombia, about
10% of the coffee berries are not harvested, resulting in berries ending up on the soil
eventually (Chamorro et al. 1995).
Understanding the dynamics of cbb in the soil is important to the development of
a control strategy. Studies carried out in Mexico (Baker 1984) and Colombia (Ruiz
1996) have demonstrated that high humidity caused by rainfall is the main trigger of
cbb emergence from fallen berries. On the other hand, soil moisture stimulates expul-
sion and death to the immature stages inside the berry (Baker et al. 1994). When the
soil is dry, the cbb remains in the berries in the soil and continues to reproduce. When
the rainy season arrives, massive adult emergence occurs.
Several attempts have been made throughout the world to use mass-produced bi-
opesticides based on entomopathogenic fungi. In Brazil, mass production of Metarhi-
zium anisopliae (Metsch.) Sorokin has resulted in an intensive use to control a
sugarcane pest, Mahanarva posticata (Stal) (Ferron 1981, Alves 1986). In several
countries of Eastern Europe, B. bassiana is recommended to control Leptinotarsa de-
cemlineata (Say) (Ferron 1981, Lipa 1990). To replace the use of chemical insecticides
due to an embargo on trade with Cuba, Cuba has been forced to move in the develop-
ment of biopesticides, especially with entomapathogenic fungi, to control different in-
sect pests (Jaffe & Rojas 1993). In Africa, international attempts to develop more
ecological control practices has resulted in the formulation of a commercial product
"green muscle" based on M. flavoviride (Gams et Rozsypal) to control several species
of the desert locust, Schistocerca gregaria Forskal (Lomer et al. 1997). In Colombia an
intensive research program with entomopathogenic fungi is been conducted to control
H. hampei (Bustillo & Posada 1996).
Beauveria bassiana (Balsamo) Vuillemin is the main natural mortality factor of
cbb and is found in all the Colombian coffee regions infested by this insect (Bustillo &

















Bustillo et al.: B. bassiana and M. anisopliae


Posada 1996, Ruiz 1996). This fungus is being investigated as a control tool in our cof-
fee IPM programs. M. anisopliae is also a potential entomopathogen that could infect
the cbb in the soil (Bernal et al. 1994). Our research was conducted to determine the
role of both B. bassiana and M. anisopliae on the regulation of cbb adult populations
that emerge from the fallen berries, and on persistence of fungi in the soil.


MATERIALS AND METHODS

This study was conducted during 1996 at the Experiment Substation Maracay of
Cenicaf6 near Armenia, Colombia. Two large plots each of 5000 m2 with 2500 coffee
plants of the Colombia variety were selected, one planting for each fungus. Soil pH
was 5.1 with an organic matter content of 12% for the B. bassiana plot andl6.5% for
the M. anisopliae plot. The experimental plots had enough susceptible green berries
in an optimal developmental stage for borer infestation. Plots contained nine trees in
square with a three-row border in all directions. The central tree of each plot served
as the sample unit. The tree was covered with a screen cage of translucid nylon cloth
to prevent movement of borers. Prior to the study, trees were left with uninfested
green berries suitable for borer infestation, and the berries on the ground were re-
moved from the soil surface beneath the trees.
B. bassiana isolate Bb 9205 originally from Diatraea saccharalis (Fabricius) and
M. anisopliae isolate Ma 9236 obtained from the CIAT fungi collection (accession
#1773) maintained in liquid nitrogen, were inoculated and then reisolated from cbb
adults and produced on rice (Antia et al. 1992). Previous studies (Bustillo & Posada
1996, Bernal et al. 1994) had shown effect of these fungi against cbb populations under
field conditions. To assure good quality of fungi produced on rice medium, concentra-
tion and viability was checked, and pathogenicity on cbb adults was performed follow-
ing the protocol established by V61ez et al. (1997). Fungal conidia were suspended in
Tween-20" and an emulsified oil Carrier" in equal parts. Water was added to the mix-
ture to give a concentration of 2 x 107 conidia/ml. The fungi were sprayed onto the
ground at the base of the trees using a volume of 50 ml/tree with a manual backpack
sprayer at a constant pressure of 40 psi, and a final dose of 1 x 10' conidia/tree.
Treatments consisted of a liquid application of fungus to the ground of the trees,
and subsequent deposition of 350 infested berries on the ground immediately after
fungal application or 2, 5, 10, 15, 20, 25 and 30 days after application. The study fol-
lowed a completely randomized design for both experiments with 10 replications and
control consisting of infestation with cbb but no fungal application. Hypothetically,
cbb emerging from the infested berries will contact the fungus. Then adults will fly to
the trees and infest the healthy berries and die from fungal infection. Infested berries
were previously disinfected with NaOC1 at 2.75% to avoid natural fungal contamina-
tion, and then dried for 12 h with the help of a fan.
Following infestation, on each tree 15 branches were randomly marked. Mycosis to
cbb was made 30 days after berry infestation by recording the number of infected and
healthy adults found in the 15 branches. The infested berries were dissected to con-
firm cbb adult mortality, and dead adults without signs of fungal infection were placed
individually in humid chambers (90% RH, 25C) for eight days to allow fungal expres-
sion on the cadavers.
To determine fungal persistence in the soil following application of conidia a dilu-
tion method was used to recover fungal propagules from the treated soil. Soil samples
were collected weekly for two months from each tree by taking 10 g of soil/tree ran-
domly from 5 sites. The 5 samples were pooled and homogenized and a subsample of
1 g was placed to reach a 10-ml suspension with sterile distilled water. From this sus-

















Florida Entomologist 82(4)


December, 1999


pension, a 10'3 dilution was prepared and two 0.1 ml aliquots were used for counting.
Isolation of B. bassiana and M. anisopliae was made using a selective media (Rivera
& L6pez 1992). This medium was prepared by adding to the one liter Saubouraud dex-
trose agar a mixture of 12 mg copper oxychloride, 26.6 pl cyproconazol and 1 ml of a
44% of lactic acid solution. Fungal spore density was estimated from the average of 10
counts per treatment and recorded as colony forming units (CFUs) /g of soil. Analysis
of variance was made and Tukey's test (P = 0.05) to determine treatment differences
using SAS statistical package version 6.11.


RESULTS AND DISCUSSION

In all treatments, coffee berry borer infestation occurred in the aerial part of the
tree as a consequence of the adult emergence from the infested berries on the soil (Ta-
bles 1 & 2). Although 350 berries were placed under each tree, different levels of in-
festation occurred in different plots. Levels of B. bassiana and M. anisopliae were
significantly higher in treatments than in controls, demonstrating that the borers
contacted the conidia in the soil. Maximum adult infection was 29.3% for B. bassiana
(Table 1) and 11% for M. anisopliae (Table 2) when cbb infestation was made 0, 2, and
5 days after fungus application. Levels of infection decreased in the subsequent treat-
ments (10, 15 and 20 days after spray), but at 25 days post-treatment an increase in
infection was detected to levels similar to the ones registered at the initial treatments.
The reason for this increase may be the conidiation of fungi on cadavers or the forma-
tion of new propagules from the existing inoculum, which is common when fungi are
sprayed into the soils, as suggested by Fargues & Robert (1985). Similar results were
found by L6pez et al. (1995) with the isolate Bb9205 ofB. bassiana active against the
cbb. Under laboratory conditions propagules of this fungus were recovered from ster-
ile and nonsterile soil even after 218 days of soil inoculation, and an unexpected in-
crease of CFUs was recorded 41 days after inoculation.


TABLE 1. BEAUVERIA BASSIANA INFECTION OF HYPOTHENEMUS HAMPEI ON COFFEE
TREES TREATED WITH FUNGAL APPLICATION TO THE SOIL.

Infestation Average Infection of Infection of Infection of
interval (days number of cbb cbb with cbb with M. cbb with
after spray) adults' + S. E3 B. bassiana (%) anisopliae (%) P. lilacinus (%)

0 551.4 + 52.3 24.7 ab2 0.1 b 0.7 b
2 221.4 + 35.9 29.3 a 0.5 a 0.2 a
5 46.8 + 6.4 21.7 abcd 0.2 b 0.1 a
10 74.3 + 9.7 10.3 cde 0.0 b 1.0 b
15 93.0 + 9.9 8.4 de 0.2 b 1.6 b
20 91.9 + 10.4 11.3 cde 0.0 b 0.8 b
25 243.8 + 24.5 24.3 abc 0.0 b 0.0.a
30 49.1 + 10.2 7.2 de 0.0 b 0.0.a
Control 170.7 18.9 6.0 e 0.0 b 0.0.a

Average number of coffee berry borers (cbb) adults in 15 branches/treated tree.
Numbers followed by the same letter do not differ significantly according to the Tukey test (P = 0.05).
Standard Error.

















Bustillo et al.: B. bassiana and M. anisopliae


TABLE 2. METARHIZIUMANISOPLIAE INFECTION OF HYPOTHENEMUS HAMPEI ON COFFEE
TREES TREATED WITH FUNGAL APPLICATION TO THE SOIL.

Infestation Average Infection of Infection of Infection of
interval (days number of cbb cbb with M. cbb with cbb with
after spray) adults' + S. E3 anisopliae (%) B. bassiana (%) P. lilacinus (%)

0 527.7 + 58.6 7.9 abc2 8.6 d 1.2 a
2 109.5 + 14.5 11.0 a 15.0 1.5 a
5 60.1 + 6.7 9.2 ab 4.5 cd 1.0 a
10 86.9 + 9.5 6.7 abc 8.8 bc 1.2 a
15 102.7 + 8.2 4.5 bc 3.4 cd 0.3 a
20 79.1 + 7.1 4.9 abc 1.8 d 0.8 a
25 250.7 + 26.2 7.7 abc 17.0 a 1.8 a
30 74.9 + 11.6 4.7 bc 3.9 cd 0.6 a
Control 207.9 + 31.2 1.7 c 4.1 cd 0.0 a

Average number of coffee berry borers (cbb) adults in 15 branches/treated tree.
Numbers followed by the same letter do not differ significantly according to the Tukey test (P = 0.05).
Standard Error.


M. anisopliae infection of cbb differed from B. bassiana in that levels of infection
were lower (Table 2). Infection fluctuated between 7.9% and 11% at 0-5 days post-
treatment but decreased gradually thereafter. Another peak of infection was reached
at the 25-day post-treatment (7.7%). These results for both B. bassiana and
M. anisopliae are similar to those reported by Miller-Kogler & Zimmermann (1986);
in studies to control L. decemlineata using B. bassiana, they found an unexpected in-
crease in number of conidia after several months of fungus spray in the soil.
The incidence of M. anisopliae and B. bassiana was measured by quantifying the
infection on H. hampei adults on the trees, but it is possible that a part of this popu-
lation is not quantified since they may die before reaching the trees and are difficult
to locate. Low levels of Infection of B. bassiana, M. anisopliae and P. lilacinus were re-
corded on cbb populations in plots where they were not sprayed (Tables 1 and 2). The
same was observed from the soil samples (Figs. 1 and 2).
It was possible to recover B. bassiana and M. anisopliae from the soil even two
months after application (Figs. 1 and 2). Interestingly, both species were recovered in
each plot; however, B. bassiana was more abundant in both plots. This can be ex-
plained by previous use of B. bassiana and M. anisopliae at this Research Station in
programs to control the borer.
No direct relationship was found between the abundance of fungi CFUs and rain-
fall, but a reduction in quantity of propagules was registered after heavy rains. In the
case of B. bassiana in the soil, two peaks were observed, one at the beginning and
other later in the experimental period, which corresponded to the high levels of fungal
infection in cbb on the trees (Fig. 1). The dynamics ofM. anisopliae in the soil was sim-
ilar to B. bassiana, but with significantly lower recovery (Fig. 2).
During soil sampling in both plots, another entomopathogen was isolated fre-
quently and identified as Paecilomyces lilacinus (Thom.) Samson by Harry C. Evans
from IIBC in England. This is the first record of this fungus attacking H. hampei adults
under natural conditions. P. lilacinus has been isolated previously from coffee soils in
Colombia with high nematode (Meloidogyne spp.) populations, to which this fungus is
















Florida Entomologist 82(4)


December, 1999


80

60

40

20


1 8 16 23 30 37 45 52 59
DAYS AFTER SPRAY

[=nBb MMa MBP1 -I rainfall


Fig. 1. Abundance (CFU/g) of Beauveria bassiana (Bb), Metarhizium anisopliae
(Ma) and Paecilomyces lilacinus (Pl) in soil treated with B. bassiana. Vertical bars
represent standard errors of the mean.

pathogenic (Cardona 1995). Although P. lilacinus was never applied, it was recovered
from the soil in higher proportion than M. anisopliae in both plots (Figs. 1 and 2).
Successful infection of susceptible soil-inhabiting insects by soil-applied ento-
mopathogenic fungi is largely dependent upon survival of an infective inoculum in the


70000
60000
d 50000
0 40000
M> 30000
20000
10000
0


1 8 16 23 30 37 45 52 59
DAYS AFTER SPRAY


m Ma i Bb H PI --- Rainfall


Fig. 2. Abundance (CFU/g) of Metarhizium anisopliae (Ma), Beauveria bassiana
(Bb) and Paecilomyces lilacinus (Pl) in soil treated with M. anisopliae. Vertical bars
represent standard errors of the mean.

















Bustillo et al.: B. bassiana and M. anisopliae


soil. This study shows that conidia of both M. anisopliae and B. bassiana can persist
for short periods of time in the soil. Other studies (Fargues & Robert 1985, Gaugler
et al. 1989, Li & Holdom 1993, Studdert et al. 1990, Su et al. 1988) have shown that
survival of these fungi may vary depending on fungal strain, type of soil, pH, micro-
bial fauna present, and soil management. Lingg & Donaldson (1981) demonstrated
that survival ofB. bassiana conidia was primarily dependent on temperature and soil
water content. In addition, microcyclic conidiation could be implicated in the high sur-
vival of conidia (Fargues & Robert 1985, Miller-Kogler & Zimmermann 1986). Due to
the high variability of conidial survival of entomopathogenic fungi, its potential as a
microbial insecticide is much greater in some soil environments than in others.
Fungal formulations play important roles in the persistence in soils. Propagules
penetrate vertically in the soil when liquid formulations are used (Storey & Gardner
1988). Recovery of CFUs from B. bassiana in treated plots was 10 times greater using
granular formulations than when liquid formulations were used (Storey et al. 1989).
The efficacy of B. bassiana and M. anisopliae to control H. hampei could be improved
by the use of more appropriate formulations such as a granular formulation. This
kind of formulation could avoid the loss of conidia trough rainfall, maintain high
conidia viability, and prevent movement from the upper layers of the soil where con-
tact with the borer takes place.

ACKNOWLEDGMENTS

We thank Agr. Eng. Luis Fernando Machado head of the Experimental Substation
Maracay of Cenicaf6 for his cooperation in the development of this research and Agr.
Eng. Anibal Arcila for his field assistance. We also want to thank Dr. Harry C. Evans
from IIBC for the kind cooperation in the identification ofPaecilomyces lilacinus and
the anonymous reviewers of this paper for the useful corrections and suggestions.

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STUDDERT, J. P., H. K. KAYA, AND J. M. DUNIWAY. 1990. Effect of water potential, tem-
perature, and clay-coating on survival of Beauveria bassiana conidia in a loam
and peat soil. J. Invertebr. Pathol. 55: 417-427.
Su, C. Y., S. S. TZEAN, AND W. H. KO. 1988. Beauveria bassiana as the lethal factor in
a Taiwanese soil pernicious to sweet potato weevil, Cylas formicarius. J. Inver-
tebr. Pathol. 52: 195-197.
VELEZ, P., F. J. POSADA, P. MARIN, M.T. GONZALEZ, E. OSORIO, YA. E. BUSTILLO. 1997.
T6cnicas para el control de calidad de formulaciones de hongos entomopat6-
genos. Boletin T6cnico No 17, Cenicaf6, Chinchind, Colombia, 37 p.

















Kerstyn & Stiling: Burn Frequency and Insect Herbivores 499

THE EFFECTS OF BURN FREQUENCY ON THE DENSITY
OF SOME GRASSHOPPERS AND LEAF MINERS
IN A FLORIDA SANDHILL COMMUNITY

ALICIA KERSTYN AND PETER STILING
Department of Biology and University Honors program, University of South Florida,
Tampa, Florida 33620-5150

ABSTRACT

The frequency and intensity of wildfires are known to affect plant diversity and
growth. We examined whether the periodicity of burning affected the density of insect
herbivores. A Florida sandhill community in West-Central Florida was divided into
ten sections, two sections of which each had a different periodicity of burning: one
year, two years, five years, seven years, and control (zero years). Each burn cycle had
been repeated many times, but all plots had been burnt in the summer of 1996, three
months prior to the onset of our study. We censused the most common herbivores of
the low-growing herbs: grasshoppers, and the most common herbivores of the trees:
leaf miners, every month for a year. Grasshoppers were counted on two common flow-
ering plants in the community, Carphephorus corymbosus (Nutt.) Torrey & A. Gray,
and Eriogronum tomentosum, Michaux. Leaf miners were counted on the two most
common trees, Quercus geminata, Small, and Quercus laevis, Walter. Grasshopper
densities were significantly higher on the flowering plants in the 1 year, 2 year, and 5
year burned plots than on the 7 year or control plots. Leaf miner densities on the oaks
were not significantly different between treatments. The differences in grasshopper
densities could be due to a higher density of forbs and the occurrence of healthier forbs
in the more frequently burned plots.

Key Words: burn frequency, Florida sandhill, oak trees, herbaceous plants, herbivore
densities

RESUME

Es bien conocido que la frecuencia e intensidad de los incendios afectan el creci-
miento y diversidad de las poblaciones de plants. En este studio se examine si la fre-
cuencia de los incendios afecta la densidad de insects herviboros. Una comunidad de
dunas de arena en la parte centro-occidental de la Florida se dividi6 en diez secciones
y en cada dos secciones se probaron las siguientes periodicidades de incendio: cada
uno, dos, cinco, siete y cero (testigo) anos. Los ciclos de incendio ya habian sido repe-
tidos en varias ocasiones anteriores, pero todos los lotes fueron incendiados en el ve-
rano de 1996, tres meses antes de comenzar este studio. Cada mes durante un ano
se hizo un censo de saltamontes (grasshoppers), los insects herviboros mas comunes
de las hierbas de porte bajo, y de minadores del follaje (leaf miners), los mas comunes
en los arboles. Los saltamontes se contaron en dos plants con flor comunes en el sitio
experimental, Carphephorus corymbosus (Nutt.) Torrey & A. Gray, y Eriogronum to-
mentosum, Michaux. Los minadores se contaron en las dos species de arboles mas co-
munes, Quercus geminata Small, y Quercus laevis Walter. Las densidades de
saltamontes fueron significativamente mas altas en las plants con flor en los lotes in-
cendiados cada uno, dos, y cinco anos, que en los lotes incendiados cada siete anos o
en los que no fueron incendiados. Las densidades de minadores en los robles no varia-
ron entire tratamientos. Las diferencias en las densidades de saltamontes podrian de-
berse a una mayor densidad de forbss" plantss herbaceas aparte de gramineas) o a la
presencia de forbs mas saludables en los lotes con mayor frecuencia de incendio.

















Florida Entomologist 82(4)


December, 1999


Periodic burning has long been known to be an integral factor in maintaining plant
diversity. Fire removes species which would otherwise smother and prevent the
growth of perennial grasses and herbaceous plants. Without fire, grass vegetation can
be replaced by woody plants (Evans 1984). In Florida, spring burnings are an impor-
tant tool in maintaining healthy sandhill communities. Sandhill requires frequent,
low intensity, fires in order to thrive and the natural burn frequency in these commu-
nities is thought to be between 1 and 10 years (Menges and Hawkes 1998). Fire stim-
ulates pine cones to release their seeds, furthermore, seeds of many species depend on
the heat of fire to germinate. Fire can also protect longleaf pines from disease caused
by fungus (Whelan 1995). In addition, the nutrients of the burned vegetation pene-
trate the soil with rainwater, providing nutrients for the remaining plants (Kozlowski
and Ahlgren 1974).
Periodic burning may directly and indirectly affect the density and richness of in-
sect herbivores by killing insects and by affecting the richness of the flora and the
quality of the vegetation, which can improve subsequent to burning because of the nu-
trient flush (Bergeron and Dansereau 1993, Mutch 1970). In this study, the effect of
fire periodicity on herbivorous insects was observed in study plots which had been
subjected to controlled burning at various intervals: seven years, five years, two years,
one year and unburned (control).


STUDY SYSTEM

The study system was a typical Florida Sandhill community dominated by
longleaf pine, Pinus palustris Mill. Deciduous oaks, such as turkey oak Quercus lae-
vis Walter, and sand live oak, Quercus geminata Small, underlie the pines, and wire-
grass, Aristida stricta Michaux, is the primary ground cover (Myers and Ewel 1990).
Turkey Oak is often stunted, up to 20m tall, but usually smaller, with long, oblong
leaves with three, five, or seven pinnate lobes. Sand live oak is a shrub or small to me-
dium-sized tree. Leaves are oblong, to elliptic, thick, and strongly revolute. Other
plants common to this landscape include: Carphephorus corymbosus (Nutt.) Torrey &
A. Gray, (Deer tongue), Eriogonum tomentosum Michaux (Dog tongue or Wild Buck-
wheat), and Serenoa repens (Bartr.) Small (Saw Palmetto). Deer tongue is a perennial
herb (Compositae) with stems up to one meter tall and with purple/lilac paint brush
flowers and lower spatulate leaves spread upon the ground. Dog tongue is a member
of the Polygonaceae and exhibits small white or pinkish flowers in terminal and sub-
terminal clusters.


MATERIALS AND METHODS

The study was conducted in the 200 ha University of South Florida Ecological Re-
search Area in Hillsborough County, Florida (28.05'N, 82.20'W) (see McCoy 1987 for
details), which contains two one hectare replicates of five burn treatments: unburned
(29 years since the last fire), one, two, five, or seven years. All the burning regimes be-
gan in 1976, except the seven year plots which began in 1975. By 1996 all regimes had
run for at least twenty-one years. The seven year plots had been burned four times,
the five year plots five times, the two year plots eleven times, and the one year plots
twenty-one times. The control plots had not been burned in at least 29 years. In 1996
every plot received a burn treatment in July. Any subsequent differences in herbivore
density between plots in 1996 and 1997 would then be attributable to the history of
burn, not the year that the plots were last burned. This provided a good opportunity
to examine the influence of fire on herbivorous insects.

















Kerstyn & Stiling: Burn Frequency and Insect Herbivores 501

Four plant species were examined for herbivores on each plot: two low-lying un-
derstory plants and two oak species. The understory species observed were Carphep-
horus corymbosus (Deer Tongue) and Eriogonum tomentosum (Dog Tongue), and the
trees were Quercus geminata (Sand Live Oak), and Quercus laevis (Turkey Oak).
The number of herbivores was counted monthly on each plant species with a vari-
ation of counting technique for each plant species. Counts consisted of visual counts of
500 leaves for each of the flowering species (about 50 plants worth), and 500 leaves for
one oak tree per plot. Most of the herbivores were sessile or unwinged juveniles that
did not fly away during censuses. Counts were made every month for 13 months, start-
ing in October, 1996 and ending in October, 1997. No fires were set in the plots during
this period. Each month a count was performed, a random selection of plants was
counted in each plot. Densities of each insect species were summed on each plot for the
year. Comparisons of burn treatments on insect densities were then made using a one-
way ANOVA on untransformed total counts, which were normally distributed.
The density of dog tongue and deer tongue on each of the plots was also deter-
mined. This was done by taking a 50 meter rope and counting the number of each of
these two plant species that it touched as it cross-sected the plot. Unfortunately, it
was not possible to collect data on plant quality in this study.


RESULTS

In this study the most common visually censused herbivores of the flowering
plants were two species of grasshoppers belonging to the genera Melanoplus and
Aptenopedes. Both species had one generation a year at our study sites with wingless
nymphs appearing in the spring and adults feeding until early fall. The most common
herbivores of the oaks were species of the leaf mining genera Buccalatrix, Stigmella,
Cameraria, and Stilbosis (Stiling and Simberloff 1991). These leaf miners were mul-
tivoltine and new mines could be found throughout the year. We therefore focused our
study on these species.
In general, grasshopper densities on the flowering plants were significantly af-
fected by burn frequency with higher numbers in one, two and five year plots than in
the seven year plots or unburned controls (Fig. 1). However, densities of leaf mining
insects on oaks were not affected by burn frequency (Fig. 2). There was no significant
difference in plant density of dog tongue or deer tongue between the treatments (dog
tongue: F,, = 3.547, P = .099; deer tongue: F,, = 1.820, P = .263). However, there was
a trend for the highest densities to occur in the more frequently burned plots (Table
1), and lack of significance may have been due to low statistical power (n = 2). This
trend was not so pronounced for dog tongue.


DISCUSSION

Grasshopper densities on both deer tongue and dog tongue were the highest in the
one year, two year and five year plots, and lowest in the seven year and control plots.
This could be caused by at least two factors. First, the host plants could simply be less
frequent in the seven year and control plots, than in the one, two or five year plots.
Second, host plant quality could vary between plots. Although there was no signifi-
cant difference in plant density between plots, the trend was for lower plant densities
in less frequently burned plots. Although we do not have data on plant quality, it is
known that fire replenishes nutrients by burning ground cover and allowing nutrients
to quickly seep into the soil (Harvey 1994, Kozlowski and Ahlgren 1974, Maclean and
Wein 1977). Protein content of prairie grasses has been shown to be higher on burned
















Florida Entomologist 82(4)


December, 1999


50-



S40



30 -

16
E 20




10-




1 2 5 7 Control
Plot Bum History

Fig. 1. Number of grasshoppers on plots with different burn periodicities (1 = 1
year, 2 = 2 years, 5 = 5 years, 7 = 7 years, control = never burned). Means and standard
errors shown. I = Melanoplus sp. on deer tongue, Carphephorus corymbosus. One
way ANOVA: F4, = 12.908, P = .008. M =Aptenopedes sp. on deer tongue. One way
ANOVA: F4, = 7.374, P = .025. = Melanoplus sp. on dog tongue, Eriogronum to-
mentosum. One way ANOVA: F4, = 7.911, P = .022. M = Aptenopedes sp. on dog
tongue. One way ANOVA: F4, =13.05, P = .007.

than on unburned areas (Owensby et al. 1970, Smith and Young 1959). The plants in
the more frequently burned (one year, two year and five year plots) appeared to us to
be healthier than those in the seven year and control plots because they were a richer
green color, the leaves were more abundant and appeared to be in better condition.
Leaf miner densities on the trees were unaffected by burn frequency, suggesting
either that any post-fire nutrient pulse was not great enough to affect tree foliage
quality or that trees behave differently to ground cover. In this regard, it is interesting
that McCullough and Kulman (1991) found that young jack pine trees on burned ar-
eas had lower foliar nitrogen than trees on unburned sites, and that jack pine bud-
worm, Choristoneura pinus Freeman, survival was related to foliar nitrogen
concentration.
We can compare and contrast our results to the few other studies that have ad-
dressed the effects of burning herbaceous vegetation on insect densities. At the Uni-
versity of Missouri Tucker Prairie Research Station, Cancelado and Yonke (1970)
found statistically greater numbers of Hemiptera and Homoptera on burned areas
over unburned areas. Similarly, Rice (1932) found that many phytophagous insects
quickly returned to burned areas because the vegetation grew more rapidly there. A
study in a prairie grassland in Kansas found that the biomass of herbivores on burned
land was significantly higher than on the unburned land and that most of the differ-
ence was caused by increased abundance of grasshoppers (Nagel 1973). Finally, a
study of postfire insect succession in southern California chaparral indicated that due
















Kerstyn & Stiling: Burn Frequency and Insect Herbivores 503

100

go

80-



750

50
20,

5 15-







1 2 5 7 Control

Plot Bum History

Fig. 2. Number of leafminers on plots with different burn periodicities (1 = 1 year,
2 = 2 years, 5 = 5 years, 7 = 7 years, control = never burned). Means and standard er-
rors shown. I I = leafminers on sand live oak, Quercus geminata. One way ANOVA:
F,5 = 1.330, P = .274. EM = leafminers on turkey oak, Quercus laevis. One way
ANOVA: F, = .407, P =.798.


to increased plant richness and diversity after chaparral fire, the insect richness and
diversity was also higher (Force 1981). These four studies, plus the present one, sug-
gest that fire increases the density of some insects, particularly grasshoppers, on her-
baceous vegetation and that increased plant quality may be the cause. Of three
exceptions that we could find, one was a study by Bulan and Barrett (1971) who found
Coleoptera, Homoptera, Hemiptera, and Diptera biomass to be significantly lower in
burned oats grassland than similar unburned areas, probably because of decreased
available producer energy and detritus. However, as Nagel (1973) points out, in nat-
ural systems burning is not likely to decrease available producer energy nearly as
much as it does in annual plant monocultures. Another exception was a study of prai-
rie grasslands in Kansas which showed forbs were killed by frequent fires and thus
the densities of grasshoppers which fed on them were reduced in frequently burned
plots, though the densities of grass-feeding grasshoppers were not (Evans 1984). This
contrasts with our study where both the density of forbs and grasshoppers were ele-
vated by fire. In does indicate, however, as Evans (1984) suggested, that grasshopper
density can be intimately linked to forb density. Finally, a study by Porter and Redak
(1997) showed reduced grasshopper density and biomass following spring burns in
California, again because host plant densities were reduced. This again is the oppo-
site to our study where the density of the forbs was increased by burning. Taken as a
whole, these studies and our results suggest that frequent fire tends to increase the
density of grasshoppers as long as it does not kill their host plants outright. This may

















Florida Entomologist 82(4)


December, 1999


TABLE 1. DENSITY OF DEER TONGUE AND DOG TONGUE PER 50M TRANSECTS ON TREAT-
MENT PLOTS WITH DIFFERENT BURN FREQUENCIES (MEANS AND STANDARD DE-
VIATION SHOWN).

Burn Plant species

Frequency years Deer tongue Dog tongue

1 35.0 + 21.2 15.2 +4.9
2 21.5+5.0 14.5+ .7
5 25.0 + 21.5 10.0+ 2.8
7 4.0 + 1.4 5.0 + 2.8
Unburned 6.5 + 2.1 7.0 + 4.2


be because of increased plant quantity and quality due to the burns or, it may be due
to lower chemical defense content of the plants. The reasons for the collapse in grass-
hopper densities between the 5 and 7 year burn regimes are not yet clear.

ACKNOWLEDGMENT

We would like to thank Henry Mushinsky and Earl McCoy whose maintenance of
the fire plots at the University of South Florida made this research possible. This re-
search was performed as part of the senior author's undergraduate honors require-
ments at the University of South Florida.

REFERENCES CITED

BERGERON, Y., AND P. R. DANSEREAU. 1993. Predicting the composition of Canadian
southern boreal forest in different fire cycles. Journal of Vegetation Science 4:
827:832.
BULAN, C., AND G. BARRETT. 1971. The effects of two acute stresses on the arthropod
component of an experimental grassland ecosystem. Ecology 52: 597-605.
CANCELADO, R., AND T. R. YONKE. 1970. Effect of prairie burning on insect popula-
tions. Journal of the Kansas Entomological Society 43: 274-81.
EVANS, E. 1984. Fire as a natural disturbance to grasshopper assemblages oftallgrass
prairie. Oikos: 9-16.
FORCE, D. 1981. Postfire insect succession in southern California chaparral. American
Naturalist: 575-582.
HARVEY, A. E. 1994. Integrated roles for insects, diseases, and decomposers in fire-
dominated forests of the inland western United States: Past, present, and fu-
ture forest health. Journal of Sustainable Forestry 2: 211-220.
KOZLOWSKI, T. T., AND C. E. AHLGREN. 1974. Fire and Ecosystems. New York: Aca-
demic Press.
MCCULLOUGH, D. G., AND H. M. KULMAN. 1991. Differences in foliage quality of young
jack pine (Pinus banksiara) on burned and clearcut sites: effects on jack pine
budworm (Choristoneura pinus pinus Freeman). Oecologia 87: 135-145.
MENGES, E. S., AND C. V. HAWKES. 1998. Interactive effects of fire and microhabitat
on plants of Florida scrub. Ecological Applications 8: 935-946.
MACLEAN, D. A., AND R. W. WEIN. 1977. Nutrient accumulation for postfire jackpine
and hardwood succession patterns in New Brunswick. Canadian Journal of
Forestry Research 7: 562-578.
McCoY, E. D. 1987. The ground-dwelling beetles of periodically burned plots of san-
dhill. Florida Entomologist 70: 31-39.

















Garcia-Aldrete & Casasola: Psocoptera from Calakmul 505

MUTCH, R. W. 1970. Wildland fires and ecosystems: A Hypothesis. Ecology 51: 1046-
1052.
MYERS, R., AND J. J. EWELL [eds.]. 1990. Ecosystems of Florida. University of Central
Florida Press: Orlando.
NAGEL, H. G. 1973. Effect of spring prairie burning on herbivorous and non-herbivo-
rous arthropod populations. Journal of the Kansas Entomological Society 46:
485-496.
OWENSBY, C. E., G. M. PAULSEN, AND J. D. MCKENDRICK. 1970. Effect of burning and
clipping on big blue stem reserve carbohydrates. Journal of Range Manage-
ment 23: 358-362.
PORTER, E. E., AND R. A. REDAK. 1997. Diet of migratory grasshopper (Orthoptera:
Acrididae) in a California native grassland and the effect of prescribed spring
burning. Environmental Entomology 26: 234-240.
RICE, L. A. 1932. Effects of fire on the prairie animal communities. Ecology 13: 392-
401.
SMITH, E. F., AND V. A. YOUNG. 1959. The effect of burning on the chemical composi-
tion of little blue stem. Journal of Range Management 12: 134-140.
STILING, P., AND D. SIMBERLOFF. 1989. Leaf abscission: induced defense against pests
or response to damage? Oikos 55: 43-49.
WHELAN, R. 1995. The Ecology of Fire. New York: Cambridge University Press, 1995.


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Garcia-Aldrete & Casasola: Psocoptera from Calakmul


PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE,
AND NEIGHBORING AREAS (CAMPECHE, MEXICO)

ALFONSO N. GARCIA ALDRETE AND J. ARTURO CASASOLA GONZALEZ
Institute de Biologia, UNAM. Departamento de Zoologia,
Apartado Postal 70- 153, 04510 Mexico, D.F. Mexico

ABSTRACT

A survey of the Psocoptera of the Calakmul Biosphere Reserve, Campeche, Mexico,
was conducted in 1997 and early 1998. The collecting effort was 260 man-hours, ex-
cluding the operation of light and Malaise traps. A total of 1675 specimens was taken,
representing 96 species, in 48 genera and 23 families. The a Diversity Index for this
collection was 22.12. Fifteen species constituted 66.7% of the total number of speci-
mens, and 40 species constituted 3.9% of the same total. Only 18 of the 96 species
present in the area are widely distributed locally, whereas 72 of the 96 species in the
area showed restricted local distribution. The level of endemism is high (19.79% of the
total number of species).

Key Words: Calakmul Biosphere Reserve, Campeche, Mexico, Psocoptera

RESUME

Durante 1997 y principios de 1998 se condujo un censo de Psocoptera en la Reserva
de la Bi6sfera de Calakmul, Campeche, en el que el esfuerzo de colecta fue de 260 ho-
ras-hombre, sin contar el tiempo de operaci6n de trampas de luz y trampas Malaise.
Fueron capturados un total de 1675 ejemplares, que representan a 96 species, en 48
generos y 23 families. El Indice de Diversidad a, calculado para 6sta colecci6n, fue de

















Florida Entomologist 82(4)


December, 1999


22.12. Quince species constituyeron el 66.7% del total de ejemplares recolectados,
mientras que 40 species constituyeron 3.9% del mismo total. S61o 18 de las 96 espe-
cies registradas en la area tienen una amplia distribuci6n local, y 72 del total de 96
species tienen una distribuci6n local muy restringida. El nivel de endemismo es alto
(19.76% del total de speciess.




The Calakmul Biosphere Reserve, in the Mexican state of Campeche, was created
on 22 May, 1989, by decree of the then President of Mexico, Carlos Salinas de Gortari.
The reserve is located at the base of the Yucatan Peninsula, in the southwestern cor-
ner of Campeche, between 17049' and 19011'N and between 89008' and 90008'W, bor-
dering on the south with the Guatemalan Peten and partially to the east with the
state of Quintana Roo. It covers approximately 7000 square kilometers, or about 14%
of the total area of Campeche. It has a peculiar shape (Fig. 1), with two large areas,
one to the north and one to the south of the highway Escarcega-Chetumal, separated
by a pronounced narrowing that crosses the highway some 15 kilometers west of X'pu-
hil. The defects in the design of the reserve have been widely pointed out and dis-
cussed by Galindo Leal (1997). All in all, it constitutes the largest humid forest
reserve area in the country, with representation, in order of importance of area cov-
ered, of medium subperennifolious forest, low subperennifolious forest, secondary
vegetation, perennifolius-subperennifolious evergreen forest, and aquatic vegetation
(Gomez Pompa & Dirzo 1995). The area is inhabited by many species of wild animals,
threatened or in danger of extinction, such as jaguar, ocelot, jaguarundi, spider and
howler monkeys, curassow, harpy eagle and tapir. The area is also rich in Mayan ar-
chaeological zones of the Classic period, in architectural styles Peten, Chenes and Rio
Bec (e.g. Calakmul, Hormiguero, Chicanna, Becan and Balamkum).
With respect to the Psocoptera fauna, the only notable reference is the record, by
Mockford & Garcia Aldrete (1996), of 26 species in Campeche, which were the result
of isolated, not systematic insect collecting in several localities in the state, none of
these in the reserve area, with only some records from the vicinities of X'puhil. Most
of the species recorded were neotropical or pantropical, widely distributed and also oc-
curring in the Caribbean.
The purpose of this work was to survey the fauna of psocids in the reserve area and
surroundings, to estimate the relative abundance and local distribution of the species
present, and to determine the specific richness of the different sites sampled. The spec-
imens collected are deposited in the National Collection of Insects (Departamento de
Zoologia, Instituto de Biologia, UNAM, Apartado Postal 70-153, 04510, Mexico, D.F.)


MATERIALS AND METHODS

In May and September, 1997, and in February, 1998, psocid collecting was con-
ducted in the reserve area and some neighboring places. The insects were taken by
beating the vegetation, sifting litter, directly examining tree trunks and rock faces,
and by using light and Malaise traps. During the first collecting event (1-9.V.1997),
the effort was of 135 man-hours, then 70 man-hours during the second collecting
event (19-25.IX.1997), and 55 man-hours during the third collecting event (15-
19.II.1998). The specimens collected were preserved directly in 80% ethanol. Table 1
presents a list of the collecting localities and their geographic coordinates, and they
are also indicated in Figure 1. It is pertinent to point out that no collecting was done
in the northern segment of the reserve, nor in the nuclear zones.

















Garcia-Aldrete & Casasola: Psocoptera from Calakmul


CALAKMUL BIOSPHERE RESERVE


Fig. 1. Location of the Calakmul Biosphere Reserve, Campeche, and Psocoptera
collecting localities in the area.


RESULTS

During the first collecting event, 708 psocid specimens were taken, with 58 species
being represented. During the second collecting event, 449 specimens were taken,
representing 41 species, 16 of which had not been taken during the first event, and
during the third collecting event, 518 specimens were taken, representing 66 species,
22 of which had not been previously collected. A total of 1675 specimens was collected,
representing 96 psocid species, in 48 genera and 23 families (Table 2).
Figure 2 shows the species accumulation curve for the collecting period. The slope
of the line indicates that a fourth collecting episode would have been needed to deter-
mine if the curve was or was not in the asymptotic phase. With the evidence that in
the third collecting event 22.9% of the total number of species were new additions, it
is likely that more unrecorded psocid species could still be found in the area.
Table 2 lists the species of psocids collected in the area, the species and number of
specimens taken in each collecting event, the relative abundance of each species, the

















Florida Entomologist 82(4)


December, 1999


TABLE 1. COLLECTING LOCALITIES IN THE CALAKMUL BIOSPHERE RESERVE AND VICINITY.

1. 25 km N of Calakmul archaeological zone, 230 m. 1817'49"N, 89050'36"W
2. Calakmul archaeological zone, ca. large "aguada", 1807'26"N, 89048'56"W
265 m.
3. Calakmul archaeological zone, 265 m. 18006'35"N, 89048'17"W
4. El Chorro, ejido Nuevo Becal, 130 m. 18035'25"N, 89015'28"W
5. Laguna de Alvarado, 316 m. 18001'54"N, 89015'45"W
6. Laguna de Alvarado, 322 m. 18000'55"N, 89016'10"W
7. Hormiguero archaeological zone, 295m. 1824'10"N, 89029'13"W
8. Arroyo Colon, ejido C. Colon, 420 m. 1812'59"N, 89027'23"W
9. San Antonio Soda, ejido Diaz Ordaz, 200 m. 1824'54"N, 89008'19"W
10. Zoh Laguna, ca. "aguada", 327 m. 18035'21"N, 89025'07"W
11. La Mancolona, ejido 20 de Junio, 232 m. 18048'38"N, 89017'29"W


amplitude of distribution in the area sampled (A = number of localities in which each
species was found), and the hierarchic order of each species (HOS), an ordering in
which the species are placed in hierarchy, according to their importance values; in this
case, the number of specimens/species was taken as importance value.
The 96 species found represent 48 genera in 23 families. The genus most diverse
is Lachesilla, with 13 species, followed by Tapinella, Caecilius andArchipsocus, each
with five species; then follow Echmepteryx, Lithoseopsis and Peripsocus, with four spe-
cies each, and Psyllipsocus, Liposcelis, Ectopsocus, Archipsocopsis, Blastopsocus and
Ptycta, with three species each. The genera Cladiopsocus, Hemipsocus and Trichade-
notecnum are represented by two species each, and there is a large group of 32 genera
represented by only one species each.
In terms of relative abundance, the 96 species are distributed in 38 ranks of hier-
archic importance (Fig. 3). The species numerically most important isArchipsocopsis
sp. 1, with 209 specimens, followed by Ectopsocus titschacki Jentsch, with 108 speci-
mens, Echmepteryx alpha Garcia Aldrete, with 92 specimens, Hemipsocus africanus
Enderlein, with 86 specimens, and Caecilius totonacus Mockford, with 78 specimens.
Together, the 15 most abundant species constitute 66.7% of the total number of indi-
viduals, and, on the opposite end, 19 species are represented by one specimen, 16 spe-
cies are represented by two specimens, and five species are represented by three
specimens, so that 40 species constitute only 3.9% of the total of specimens collected.
The a Diversity Index [S = a log (1 + N/a), cf. Taylor, Kempton & Woiwod (1976)],
calculated for the Calakmul psocid collection, resulted in a value of 22.12, one of the
highest recorded in the literature, surpassed only by the diversity indices for the Pso-
coptera of Chamela, Jalisco, Mexico (a = 24.01, N = 2863, S = 115), Panama Lowlands
(c = 24.5, N = 10092, S = 148), and Los Tuxtlas, Veracruz, Mexico (a = 32.45, N = 4194,
S = 158) (Broadhead & Wolda 1985; Garcia Aldrete 1988; Garcia Aldrete, Mockford &
Garcia Figueroa 1997).
Table 3 presents the species and number of specimens of each species collected in
each locality during this study; it also includes the habitats in which the species were
collected. Since the collecting effort was not the same in each locality, the results are
biased; however, the comparatively high species richness of localities 3, 7 and 10 prob-
ably reflect also intrinsic differences among the localities sampled. The richer ones are
sites physically complex, varied, with several habitats sampled, such as the Calakmul
archaeological zone, the Hormiguero archaeological zone or Laguna de Alvarado.






















TABLE 2. PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PERCENTAGE OF THE
TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).

1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS


TROGIOMORPHA

Lepidopsocidae
1 Thylacella cubana (Banks), 1941
2 Nepticulomima Enderlein, 1906
3 Proentomum personatum
Badonnel, 1949
4 Soa flaviterminata
Enderlein, 1906
5 Echmepteryx alpha Garcia Aldrete,
1984
6 E. falco Badonnel,1949
7 E. madagascariensis (Kolbe), 1885
8 E. intermedia Mockford, 1974
9 Neolepolepis caribensis (Turner),
1975

Psoquillidae
10 Rhyopsocus sp.


7 12

1 7


1 4


1 5 0,30 4 34 9
21 1,25 2 19
0
3 6 43 2,57 10 12

1 9 0,54 3 30 |

13 6 92 5,49 7 3
12 0,72 2 27
5 24 66 3,94 3 7
2 3 17 1,01 4 23

3 0,18 1 36


1 0,06 1 38






















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).

1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS


Psyllipsocidae
11 Psyllipsocus Selys-Longchamps,
1872. sp. 1
12 P.sp.2
13 P. sp.3

TROCTOMORPHA

Amphientomidae
14 Lithoseopsis Mockford, 1993. sp. 1
15 L. sp.2
16 L. sp. 3
17 L. sp.4

Compsocidae
18 Electrentomopsis variegatus
Mockford, 1967

Liposcelididae
19 Belaphopsocus badonneli New, 1971
20 Embidopsocus cubanus Mockford,
1987


12 14


3 9


2 1
1 1
8 4


1 1


3 1 36 2,15 3 13
5 18 1,07 3 22
1 1 0,06 1 38




1 4 20 1,19 5 20 2
2 0,12 1 37
12 0,72 1 27 00
1 1 0,06 1 38 4



1 1 2 0,12 1 37


2 2 0,12 1 37
2 0,12 1 37




















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).


1-9. V. 1997 19-25. IX. 1997 15-19
(135 man hours) (70 man hours) (55 m

males females nymphs males females nymphs males fen

21 Liposcelis bostrychopila Badonnel,


1931
22 L. ornata Mockford, 1978
23 Liposcelis Motschulsky, 1852
24 Nanopsocus oceanicus Pearman,
1928
25 Tapinella maculata Mockford &
Gurney, 1926
26 T olmeca Mockford, 1975
27 T vittata Garcia Aldrete, 1993
28 Tapinella Enderlein, 1908. sp. 1
29 T sp. 2
30 Pachytroctes ixtapaensis Garcia
Aldrete, 1986

PSOCOMORPHA

Epipsocidae
31 Epipsocus Hagen, 1866

Dolabellopsocidae
32 Dolabellopsocus roseus Eertmoed,
1973


2 6 2 2 3
4 25 5 1 6
2 17 3 4


2


2 3


. II. 1998
an hours)

tales nymphs N %T A HOS

2 2 0,12 2 37

1 3 0,18 2 36
1 0,06 1 38
?
6 21 1,25 3 19
0
15 0,90 7 24 .
2 44 2,63 6 10
23 2 53 3,16 6 10
4 19 1,13 6 21
3 11 0,66 3 28

1 3 4 0,24 1 35 3




1 6 0,36 2 33


1 0,06 1 38






















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).

1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS


Cladiopsocidae
33 Cladiopsocus garciai Eertmoed,
1986
34 C. ocotensis Garcia Aldrete, 1996

Ptiloneuridae
35 Loneura leonilae Garcia Aldrete,
1995
36 Triplocania spinosa Mockford, 1957

Asiopsocidae
37 Notiopsocus Banks, 1913

Caeciliidae
38 Caecilius casarum Badonnel, 1931


39
40
41
42


C. totonacus Mockford, 1966
Caecilius Curtis, 1837. Sp. 1
C. sp. 2
Xanthocaecilius Mockford, 1989


Amphipsocidae
43 Dasypsocus roesleri (New &
Thornton), 1975


1 4 3


1 4 3 8 0,48 2 31
1 1 3 13 0,78 2 26
FL


2 0,12 1 37
3 5 7 15 0,90 2 24



00
3 7 11 0,66 2 28 .
co

2 0,12 1 37
79 4,72 3 5
1 4 4 9 0,54 3 30
1 1 0,06 1 38 g
1 0,06 1 38
CD
3 13 25 1,49 4 18 "-

-------------------------------CO


1 51 27


1 1 7




















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).


1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS


Lachesillidae
44 Anomopsocus Roesler, 1940
45 Nanolachesilla Mockford &
Sullivan, 1986
46 Lachesilla bottimeri Mockford &
Gurney, 1956
47 L. bifurcata Garcia Aldrete, 1986
48 L. sp. (forcepeta group) 2 5
49 L. cuala Garcia Aldrete, 1988
50 L. denticulata Garcia Aldrete, 1988 3 2
51 L. disjuncta Garcia Aldrete, 1988 1 7
52 L. nuptialis Badonnel & Garcia
Aldrete, 1980 5
53 L.penta Sommerman, 1946 1 3
54 L. riegeli Sommerman, 1946 1 1
55 L. tropica Garcia Aldrete, 1982 3 1
56 L. yanomamioides Garcia Aldrete,
1996 2 2


57 Lachesilla Westwood, 1840. sp. F9 B
58 L. sp. (pedicularia group)


1 2


1 0,06 1 38

1 0,06 1 38


1


3 2 3 1



16


7
2 8
1
3


1 0,06 1 38
1 1 0,06 1 38
3 13 32 1,91 6 14
2 2 0,12 1 37
5 18 35 63 3,76 5 8
1 1 1 27 1,61 4 16


10
3 9


28 1,67 8 15
44 2,63 7 11
3 0,18 2 36
8 0,48 6 31


9 4 7 7 6 15 26 78 4,66 6 6
2 2 7 11 0,66 1 28
3 1 4 11 0,66 7 28





















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).

1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS


Ectopsocidae
59 Ectopsocus mexicanus Garcia
Aldrete, 1991
60 E. titschacki Jentsch, 1929 1i'
61 E. vilhenai Badonnel, 1955 4

Peripsocidae
62 Peripsocuspotosi Mockford, 1971
63 P. chamelanus Badonnel, 1986
64 P. ca. stagnivagus Chapman, 1930
65 P. sp. 1

Archipsocidae
66 Archipsocopsis Badonnel, 1966. sp. 1 1
67 A. sp. 2
68 A. sp. 3 1
69 Archipsocus Hagen, 1882 sp. 1
70 A. sp. 2
71 A. sp. 3 1
72 A. sp.4
73 A. sp. 5


45 12 10 16 2


1 1 0,06 1
2 3 1 108 6,45 7
10 0,60 3


0,30
0,12
0,12
0,18


2 8 101
1


7 1


4 1


1 209 12,48
7 0,42
2 0,12
2 0,12
33 11 57 3,40
2 0,12
2 0,12
1 0,06




















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).


1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours

males females nymphs males females nymphs males females nyi

74 Pseudarchipsocus guajiro 1 2


Mockford, 1974
Pseudocaeciliidae
75 Pseudocaecilius citricola
(Ashmead), 1879
76 Heterocaecilius badonneli Garcia
Aldrete, 1989
77 Scytopsocus Roesler, 1940 (ca. coria-
ceous Roesler, 1940)
Philotarsidae
78 Haplophallus Thornton, 1959
79 Aaroniella Mockford, 1951
Elipsocidae
80 Palmicola Mockford, 1955
81 Nepiomorpha brasiliana Badonnel,
1973
Hemipsocidae
82 Hemipsocus africanus Enderlein,
1907
83 H. pretiosus Banks, 1930


4 6 4


2 1


1
1


1 1


1 14


6 13
2


7 12 28 14


8
) a

mphs N %T A HOS

3 0,18 1 36

Ct


2 7 0,42 4 32

14 0,84 1 25
a-
3 7 0,42 3 32


3 6 0,36 3 33
1 2 0,12 1 37


2 0,12 2 37

15 0,90 2 24



86 5,13 5 4
8 0,48 1 31 at






















TABLE 2. (CONTINUED) PSOCOPTERA FROM THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE AND VICINITY (N = NUMBER OF SPECIMENS, %T = PER-
CENTAGE OF THE TOTAL, A = NUMBER OF LOCALITIES IN WHICH EACH SPECIES WAS COLLECTED, HOS = HIERARCHIC ORDER OF SPECIES).

1-9. V. 1997 19-25. IX. 1997 15-19. II. 1998
(135 man hours) (70 man hours) (55 man hours)

males females nymphs males females nymphs males females nymphs N %T A HOS

Psocidae


84 Blastopsocus Roesler, 1943. Sp.1
85 B. sp. 2
86 B. sp. 3
87 Cerastipsocus trifasciatus
(Provancher), 1876
88 Metylophorus Pearman, 1932


89
90


1 1


Steleops Enderlein, 1910
Ptycta Enderlein, 1925. sp. 1


91 P. sp. 2
92 P. tikal


a (Mockford), 1957


93 Trichadenotecnum Enderlein, 1909.
sp. 1
94 T sp. 2
Myopsocidae
95 Lichenomima varia (Navas), 1927
96 Myopsocus Hagen, 1866
TOTAL
TOTAL
a DIVERSITY INDEX (S a log(1


1 2


15 9 1 1


5 1


76 423
711
22,12


212 68


256 122
446


2 2 5 0,30 3 34
1 16 18 1,07 2 22
1 1 0,06 1 38

14 17 1,01 3 23
1 1 0,06 1 38
1 0,06 1 38
1 0,06 1 38
1 1 0,06 1 38
1 0,06 1 38
0o

1 1 2 5 0,30 2 34 S


4 0,24 2 35


26 1,55 2 17
9 0,54 4 30
CD
1675

(C


50 240 228
518

















Garcia-Aldrete & Casasola: Psocoptera from Calakmul


120



100



S80-



5 60-

E
z 40-



20-



0
V. 1997 IX. 1997 II. 1998
Collecting events

Fig. 2. Species accumulation curve for the Psocoptera of the Calakmul area. May
1997-February 1998.


The species of psocids collected in the Calakmul area, can be assigned to the fol-
lowing biogeographic categories:

I. Endemics and presumed endemics (19 species).
Nepticulomima sp., Rhyopsocus sp., Psyllipsocus sp. 2, Lithoseopsis sp. 4,
Liposcelis sp., Tapinella sp. 1, Xanthocaecilius sp., Nanolachesilla sp.,
Peripsocus sp. 4, Archipsocopsis sp. 3, Palmicola sp., Blastopsocus spp.l, 2,
and 3, Metylophorus sp., Steleops sp., Ptycta sp.1, and Trichadenotecnum
spp. 1 and 2.

II. Tropical waifs (9 species).
Proentomum personatum Badonnel, Soa flaviterminata Enderlein, Echme-
pteryx falco Badonnel, E. madagascariensis (Kolbe), Nanopsocus oceanicus
Pearman, Ectopsocus titschacki Jentsch, E. vilhenai Badonnel, Pseudocae-
cilius citricola (Ashmead) and Hemipsocus africanus Enderlein.

III. Cosmopolitan species (2 species).
Liposcelis bostrychophila Badonnel, Caecilius casarum Badonnel.

IV. Species widespread in tropical and subtropical America (9 species).
Thylacella cubana (Banks), Belaphopsocus badonneli New, Liposcelis or-
nata Mockford, Tapinella maculata Mockford & Gurney, Dasypsocus

















Florida Entomologist 82(4)


December, 1999


6.00



5.00



4.00



Ln 3.00 "



2.00



1.00



0.00
0 20 40 60 80 100 120

Species sequence

Fig. 3. Species abundance distribution of the collection of Psocoptera from the
Calakmul Biosphere Reserve and surrounding areas. Log. of abundance ranked
against species. a = 22.12.

roesleri (New & Thornton), Lachesilla cuala Garcia Aldrete, Peripsocus po-
tosi Mockford, Nepiomorpha brasiliana Badonnel, and Cerastipsocus trifas-
ciatus (Provancher).

V. Species occurring in Mexico and southeastern USA (2 species).
Lachesilla bottimeri Mockford & Gurney, L. penta Sommerman.

VI. Species occurring in tropical Mexico and Guatemala or Belize, not extending to
Central America and the Caribbean (7 species).
Echmepteryx alpha Garcia Aldrete, Cladiopsocus garciai Eertmoed, Triplo-
cania spinosa Mockford, Anomopsocus sp. a, Lachesilla disjuncta Garcia Al-
drete, L. nuptialis Badonnel & Garcia Aldrete, Ptycta tikala Mockford.

VII. Species occurring in tropical Mexico, Central America and the Caribbean (2 spe-
cies).
Lachesilla denticulata Garcia Aldrete, L. riegeli Sommerman.

VIII. Species occurring in tropical Mexico and the Caribbean (5 species).
Echmepteryx intermedia Mockford, Neolepolepis caribensis (Turner), Tap-
inella olmeca Mockford, Lachesilla yanomamioides Garcia Aldrete, Hemip-
socus pretiosus Banks.





















TABLE 3. PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH LOCALITY, AND
HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE TRUNKS AND
BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS PLANTS. VIII.
CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

TROGIOMORPHA
Lepidopsocidae
1 Thylacella cubana
(Banks), 1941 2 1 1* *
2 Nepticulomima
Enderlein, 1906 17 4 *
3 Proentomum
personatum
Badonnel, 1949 2 11 1 1 12 2 1 1 5 7 *
4 Soa flaviterminata
Enderlein, 1906 5 1 3 *
5 Echmepteryx alpha
Garcia Aldrete, 1984 12 23 10 5 29 6 7 *
6 E. falco
Badonnel, 1949 6 6 *
7 E. madagascariensis
(Kolbe), 1885 14 45 7 *
8 E. intermedia 3 5 5 4 *
Mockford, 1974






















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH K.
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

9 Neolepolepis 3
caribensis (Turner),
1975 0

Psoquillidae
10 Rhyopsocus sp. 1

Psyllipsocidae
11 Psyllipsocus
Selys-Longchamps,
1872. sp. 1 12 11 13 *
12 P.sp.2 7 9 2 *
0o
13 P.sp.3 1 *

TROCTOMORPHA

Amphientomidae
14 Lithoseopsis (
Mockford, 1993. sp. 1 2 1 13 2 2 *
15 L. sp. 2 2 *
16 L. sp. 3 12 *
17 L.sp.4 1 *





















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II II IV V VI VII VIII IX X XI

Compsocidae
18 Electrentomopsis var-
iegatus Mockford,
1967 2

Liposcelididae
19 Belaphopsocus badon-
neli New, 1971 2
20 Embidopsocus cuba-
nus Mockford, 1987 2
21 Liposcelis bostrycho-
pila Badonnel, 1931 1 1 *
22 L. ornata Mockford,
1978 2 1 *
23 Liposcelis Motschul-
sky, 1852 1
24 Nanopsocus oceani-
cus Pearman, 1928 18 1 2* *
25 Tapinella maculata 1 5 1 5 1 1 1 *
Mockford & Gurney,
1926





















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH C1
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

26 T olmeca Mockford, 16 18 2 6 1 1
1975
27 T vittata Garcia
Aldrete, 1993 4 27 1 8 9 4 *
28 Tapinella Enderlein,
1908. sp. 1 2 1 1 2 10 3 *
29 T sp. 2 7 1 3 *
30 Pachytroctes ixtapaen-
sis Garcia Aldrete,
1986 4 *

PSOCOMORPHA
oo
Epipsocidae
31 Epipsocus Hagen,
1866 1 5

Dolabellopsocidae
32 Dolabellopsocusroseus
Eertmoed, 1973 1 *
Cladiopsocidae
33 Cladiopsocus garciai 7 1 *
Eertmoed, 1986
------------------------------------------------------------------------------------ C




















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II II IV V VI VII VIII IX X XI

34 C. ocotensis Garcia 5 8 *
Aldrete, 1996

Ptiloneuridae
35 Loneura leonilae
Garcia Aldrete, 1995 2 *
36 Triplocania spinosa
Mockford, 1957 14 1 *

Asiopsocidae
37 Notiopsocus Banks,
1913 9 2

Caeciliidae
38 Caecilius casarum
Badonnel, 1931 2
39 C. totonacus
Mockford, 1966 1 69 9 *
40 Caecilius Curtis,
1837. sp. 1 6 1 2 *
41 C. sp. 2 1 *
42 Xanthocaecilius 1 *
Mockford, 1989






















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II II IV V VI VII VIII IX X XI

Amphipsocidae
43 Dasypsocus roesleri
(New & Thornton),
1975 2 18 2 3 *

Lachesillidae
44 Anomopsocus
Roesler, 1940 1
45 Nanolachesilla Mock-
ford & Sullivan, 1986 1 *
46 Lachesilla bottimeri
Mockford & Gurney,
1956 1 *
47 L. bifurcata Garcia
Aldrete, 1986 1 *
48 L. sp. (forcepeta
group) 2 14 6 5 4 1 *
49 L. cuala Garcia
Aldrete, 1988 2 *
50 L. denticulata 4 29 1 23 6 *
Garcia Aldrete, 1988






















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.


Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

E1 LT t;. 4 i 7 17 1 *


sjunc a arc a
Aldrete, 1988
52 L. nuptialis Badonnel
& Garcia Aldrete, 1980
53 L. penta
Sommerman, 1946
54 L. riegeli
Sommerman, 1946
55 L. tropical Garcia
Aldrete, 1982
56 L. yanomamioides
Garcia Aldrete, 1996
57 Lachesilla Westwood,
1840. sp. F9B
58 L. sp. (pedicularia
group)

Ectopsocidae
59 Ectopsocus mexicanus
Garcia Aldrete, 1991
60 E. titschacki Jentsch,
1929


2 6 1 1 3 5


5 3


10 22


19 2 3


9 1 *

6 6 *

1 *


1 1 1 1 1 3

1 37 2 6


1 3 2


2 1 1 1


19 11 4 6 40 10


Ct

Q

t
0
P
S
0
t t Cb
0
Ct


0


* *


A


S`


L, I


-LIr -


18 *






















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II II IV V VI VII VIII IX X XI

61 E. vilhenai 3 2 5
Badonnel, 1955


Peripsocidae
62 Peripsocus potosi
Mockford, 1971
63 P. chamelanus
Badonnel, 1986
64 P. ca. stagnivagus
Chapman, 1930
65 P. sp. 1

Archipsocidae
66 Archipsocopsis
Badonnel, 1966. sp. 1
67 A. sp. 2
68 A. sp. 3
69 Archipsocus Hagen,
1882 sp. 1
70 A. sp. 2
71 A. sp. 3


3 *

1 *


1 1 *
1 2 *



1 1 8 47 1 18 13 *
5 2 3


1 9 1 2 2 2 1 3 36





















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

72 A. sp.4 1 1
73 A. sp. 5 1
74 Pseudarchipsocus gua-
jiro Mockford, 1974 3

Pseudocaeciliidae
75 Pseudocaecilius citri-
cola (Ashmead), 1879 1 1 1 4
76 Heterocaecilius ba-
donneli Garcia
Aldrete, 1989 14
77 Scytopsocus Roesler,
1940 (ca. coriaceous
Roesler, 1940) 3 3 1

Philotarsidae
78 Haplophallus Thorn-
ton, 1959 1 1 4
79 Aaroniella 2 *
Mockford, 1951






















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI


Elipsocidae
80 Palmicola
Mockford, 1955
81 Nepiomorpha brasili-
ana Badonnel, 1973

Hemipsocidae
82 Hemipsocus africa-
nus Enderlein, 1907
83 H. pretiosus Banks,
1930

Psocidae
84 Blastopsocus Roesler,
1943. Sp.1
85 B. sp.2
86 B. sp. 3
87 Cerastipsocus trifas-
ciatus (Provancher),
1876
88 Metylophorus
Pearman, 1932


1 1


1 58


6 16 5


1 *
4 *


3 13


o
a-




* 0









tl



(0





















TABLE 3. (CONTINUED) PSOCOPTERA OF THE CALAKMUL BIOSPHERE RESERVE, CAMPECHE, AND VICINITY. NUMBER OF SPECIES TAKEN IN EACH
LOCALITY, AND HABITATS IN WHICH EACH SPECIES WAS COLLECTED. I. BRANCHES AND FOLIAGE OF SHRUBS. II. LEAF LITTER. III. TREE
TRUNKS AND BARK. IV. TYPHA FOLIAGE. V. DEAD PALM FRONDS. VI. BROMELIADS, ORCHIDS AND OTHER EPIPHYTES. VII. HERBACEOUS
PLANTS. VIII. CALCAREOUS ROCK FACES. IX. ABANDONED TERMITE NEST. X. MALAISE TRAP. XI. LIGHT TRAP.

Localities Habitats

1 2 3 4 5 6 7 8 9 10 11 I II III IV V VI VII VIII IX X XI

89 Steleops Enderlein, 1 *
1910
90 Ptycta Enderlein,
1925. sp. 1 1
91 P. sp. 2 1
92 P. tikala (Mockford),
1957 1
93 Trichadenotecnum
Enderlein, 1909. sp. 1 4 1
94 T sp. 2 3 1 *

Myopsocidae
95 Lichenomima varia
(Navas), 1927 25 1 *
96 Mo socus Hagen, 2 4 2 1 *


Number of species 5 25 57 16 22 25 50 10 13 36 6 62 19 22 4 21 21 7 20 3 22 11

Number of individuals 7 126 408 110 102 231 290 29 59 298 15

















Florida Entomologist 82(4)


December, 1999


IX. Species occurring in tropical Mexico and Central America (5 species).

Caecilius totonacus Mockford, C. sp. 3, Lachesilla tropica Garcia Aldrete,
Scytopsocus ca. coriaceous Roesler, Lichenomima varia (Navas).

X. Species restricted to the Yucatan Peninsula (5 species).

Psyllipsocus spp. 1 and 3, Lithoseopsis sp. 1, Loneura leonilae Garcia Al-
drete, Ptycta sp. 2.

XI. Species occurring in the Yucatan Peninsula and neighboring areas (6 species).

Lithoseopsis spp. 2 and 3, Archipsocus sp. 1, Heterocaecilius badonneli Gar-
cia Aldrete, Aaroniella sp., Myopsocus sp.

XII. Species occurring in tropical Mexico (20 species).

Electrentomopsis variegatus Mockford, Tapinella vittata Garcia Aldrete,
Pachytroctes ixtapaensis Garcia Aldrete, Epipsocus sp., Dolabellopsocus ro-
seus Eertmoed, Cladiopsocus ocotensis Garcia Aldrete, Caecilius sp. 2,
Lachesilla bifurcata Garcia Aldrete, L. sp. (forcepeta group), L. pedicularia
group, Ectopsocus mexicanus Garcia Aldrete, Peripsocus chamelanus Ba-
donnel, P. ca. stagnivagus Chapman, Archipsocopsis spp. 1 and 2, Archipso-
cus spp. 2, 3, 4, and 5, Haplophallus sp.

XIII. Species occurring in Cuba (2 species).

Embidopsocus cubanus Mockford, Pseudarchipsocus guajiro Mockford.

XIV. Species restricted to Guatemala or Belize (3 species).

Tapinella sp. 2, Notiopsocus sp., Lachesilla F9B.


Given the geographic location of Calakmul, the composition of its psocid fauna
does not contain elements of surprise and it is rather as expected for an area near the
edge of tropical Mexico, and close to Central America and the Caribbean; it is domi-
nated by Mexican tropical species, with the addition of the species widespread in trop-
ical America, plus the species also shared with Central America and the Caribbean
region, plus the usual array of tropical waifs and cosmopolitans. Categories IX and X,
of species restricted to the Yucatan Peninsula or occurring nearby, point to the biotic
distinctness of that area (see also Barrera 1962). The category of endemics, compris-
ing 19.79% of the fauna of Calakmul, gives it the element of uniqueness. It is perti-
nent to note that 18 of the 26 species previously recorded in Campeche, were found in
the area of the Calakmul Reserve.
The results of this survey indicate that the psocid community of the Calakmul Bio-
sphere Reserve area is rich in species, with a high proportion of endemics. It also indi-
cates that the community shows fragility in that there is a large number of "rare"
species (e.g. 40 species of which only 1-3 specimens were collected throughout the sam-
pling period), and in that a large number of species have only a small amplitude of local
distribution (e.g. 72 species collected in only one or two localities), with which environ-
mental changes, either natural or anthropogenic, could result in local extinctions.

















Garcia-Aldrete & Casasola: Psocoptera from Calakmul 531

ACKNOWLEDGEMENTS

This project is part of a larger one, financed by the Mexican agency CONABIO
(Project M003 "Reconocimiento de la biodiversidad de la Reserva de la Bi6sfera Calak-
mul: Odonata, Psocoptera y Diptera Acuaticos (Insecta)"). Atilano Contreras, Enrique
Gonzalez, Tomas Martinez, Adolfo Ibarra, and Rocio Lopez participated in it and con-
tributed with specimens of Psocoptera. To all of them, and to CONABIO, our most sin-
cere thanks.


REFERENCES CITED

BARRERA, A. 1962. La peninsula de Yucatan como provincia bi6tica. Revista de la So-
ciedad Mexicana de Historia Natural 23: 71-105.
BROADHEAD, E., AND H. WOLDA. 1985. The diversity of Psocoptera in two tropical for-
ests in Panama. Journal of Animal Ecology 54: 739-754.
GALINDO-LEAL, C. 1997. Disefo de reserves: el "mal cong6nito" de Calakmul. Ecotono.
Centro para la biologia de la conservaci6n. Boletin del Programa de Investi-
gaci6n Tropical. Stanford University. Pp.4-7.
GARCIA ALDRETE, A. N. 1988. The psocids (Psocoptera) of Chamela, Jalisco, Mexico.
Species, diversity, abundance distribution and seasonal changes. Folia Entomo-
logica Mexicana 77: 63-84.
GARCIA ALDRETE, A. N., E. L. MOCKFORD, AND J. GARCIA FIGUEROA. 1997. Psocoptera,
p. 299-309 in Gonzalez Soriano, E., R. Dirzo, and R. Vogt. Historia Natural de
Los Tuxtlas. Institute de Biologia-Instituto de Ecologia, UNAM. Mexico.
GOMEZ POMPA, A., AND R. DIRZO. 1995. Reservas de la bi6sfera y otras areas naturales
protegidas de M6xico. Institute Nacional de Ecologia (SEMARNAP)- CONA-
BIO. Mexico, D. F. 159 pp.
MOCKFORD, E. L., AND A. N. GARCIA ALDRETE. 1996. Psocoptera, p. 175-205 in
Llorente, B. J., A. N. Garcia Aldrete, and E. Gonzalez S. Biodiversidad, tax-
onomia y biogeografia de artr6podos de M6xico. Institute de Biologia, UNAM.,
Mexico.
TAYLOR, L. R., R. A. KEMPTON, AND I. P. WOIWOD. 1976. Diversity statistics and the
log-series model. Journal of Animal Ecology 45: 255-272.

















Florida Entomologist 82(4)


December, 1999


DEVELOPMENT OF PARASITOID INOCULATED SEEDLING
TRANSPLANTS FORAUGMENTATIVE BIOLOGICAL CONTROL
OF SILVERLEAF WHITEFLY (HOMOPTERA: ALEYRODIDAE)

JOHN A. GOOLSBY'2 AND MATTHEW A. CIOMPERLIK1
1USDA-APHIS-PPQ- Mission Biological Control Center,
P.O. Box 2140, Mission, TX 78573

2PRESENT ADDRESS: USDA-ARS Australian Biological Control Laboratory,
PMB#3, Indooroopilly, QLD, Australia 4068

ABSTRACT

Methods are presented for producing banker plants, transplants that are used for
augmentation ofEretmocerus parasitoids for biological control ofBemisia argentifolii
in cucurbit crops. Preference tests were conducted with B. argentifolii and its parasi-
toid Eretmocerus hayati for ten cantaloupe varieties to determine their suitability for
use as banker plants. Bemisia argentifolii showed a significant preference for the va-
rieties Copa de Oro and Mission, whereas, E. hayati showed the greatest preference
for Copa de Oro, Mission and Primo. The impact of imidacloprid on the development
of parasitoid immatures on banker plants was evaluated. Thirteen days after release
ofE. hayati, banker plants treated with imidacloprid produced equivalent numbers of
parasitoids as did control plants. Field trials, incorporating the use of banker plants
and imidacloprid, were conducted for two seasons in spring cantaloupes and one sea-
son in fall watermelons. Numbers of parasitoid progeny produced per cantaloupe
banker plant were approximately 94.6 and 102.1 in two trials during the Spring of
1997 and 1998. Field release rates per acre in cantaloupe were estimated to be 68,946
and 29,970 for the 1997 and 1998 trials, with banker plants incorporated with regular
transplants at a ratio of 1:10 and 1:30 respectively. In the watermelon trial, the mean
number of parasitoid progeny produced per banker plant was determined to be 94.6,
with an estimated 4156 released per acre with a ratio of 1:30 banker to regular trans-
plants. Banker plants were shown to be a reliable method for field delivery of Eret-
mocerus parasitoids in transplanted and direct seeded cantaloupe or watermelon
crops. The methods used to produce parasitoid inoculated banker plants are dis-
cussed.

Key Words: augmentation, parasitoids, Eretmocerus hayati, Bemisia argentifolii, im-
idacloprid

RESUME

Se discuten m6todos para la producci6n de "banker plants", transplants en los
que se liberan parasitoides de Eretmocerus, para el control biol6gico de la mosca
blanca, Bemisia argentifolii (= B. tabaci biotipo B) en cucurbitaceas. Se realizaron
pruebas de preferencia con B. argentifolii y su parasitoide Eretmocerus hayati en 10
cvs. de mel6n "cantaloupe" para determinar la efectividad de esta plant como banker.
B. argentifolii mostr6 una preferencia significativa por los cvs. Copa de Oro y Mission,
mientras que E. hayati mostr6 preferencia por Copa de Oro, Mission y Primo. Se eva-
lu6 el impact de imidacloprid en el desarrollo de parasitoides inmaduros en plants
banker. Trece dias despues de la liberaci6n de E. hayati, las plants banker tratadas
con imidacloprid produjeron la misma cantidad de parasitoides que las plants no tra-
tadas. Se llevaron a cabo experiments de campo usando plants banker e imidaclo-
prid durante dos temporadas en melones de primavera y durante una temporada en
sandia de otono. La progenie de parasitoides producida por cada plant de mel6n

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 533

banker fue de 94.6 y 102.1 en dos ensayos efectuados durante la primavera de 1997 y
1998. En mel6n, la tasa de liberaci6n en campo por acre se estim6 en 68,946 y 29,970
para los ensayos efectuados en 1997 y 1998, en los cuales se incorporaron plants
banker en proporci6n de 1:10 y 1:30, respectivamente. En sandia, la progenie de pa-
rasitoides promedio por plant banker fue 94.6. La cantidad de parasitoides liberada
por acre se estim6 en 4,156, con una proporci6n de plants banker de 1:30. El uso de
plants banker represent un metodo confiable para la distribuci6n de parasitoides
Eretmocerus en el campo, tanto en mel6n o sandia de transplant o siembra direct.
Se discuten los metodos empleados para la producci6n de plants banker inoculadas.





Bemisia argentifolii (=Bemisia tabaci Biotype B), Silverleaf whitefly (SLWF), con-
tinues to be a serious pest of annual row crops such as cotton, cole crops, cucurbits,
okra, sesame, and tomato, in the subtropical growing areas across the US and world-
wide (DeQuattro 1997, Legaspi et al. 1997, Riley & Ciomperlik 1997). Damage is
caused not only by direct feeding but also through transmission of geminiviruses
(Brown & Bird 1992, Brown 1994, Polsten & Anderson 1997). Estimates of the mon-
etary costs to U.S. agriculture due to crop loss, job displacement and cost of control are
now approaching one billion dollars (Bezark 1995, De Barro 1995, Henneberry et al.
1996). Imidacloprid has temporarily reduced the impact of Bemisia in some crops,
however resistance is now documented (Prabahker et al. 1997). Silverleaf whitefly
control strategies are needed which decrease dependence on single control tactics. To
this end, over 38 exotic populations of Bemisia parasitoids from 16 countries have
been imported and evaluated in a comprehensive multi-state, multi-crop biological
control program (Kirk et al. 1993, Nguyen & Bennett 1994, Goolsby et al. 1996,
Goolsby et al. 1998, Rose & Zolnerowich 1998). Recently, imported exotic Eretmocerus
spp. have been integrated with selective insecticides and cultural controls into a bio-
logical control based Integrated Pest Management (BC-IPM) program (Ciomperlik et
al. 1997). This strategy is proposed as the basis for long term sustainable manage-
ment of silverleaf whitefly.
Several biological control strategies including importation of new natural enemies
(classical), natural enemy refugia (conservation), and inoculative releases (augmen-
tation) have been evaluated for management of B. argentifolii (Roltsch & Pickett
1995, Carruthers et al. 1996, Corbett 1996, Henneberry et al. 1996, Simmons et al.
1997, Ciomperlik et al. 1997). Implementation of biological control strategies has
been difficult in the subtropical agricultural areas where the impact ofB. argentifolii
is most severe. Several reasons may account for this difficulty such as: discontinuity
of annual crops, high use of pesticides for other pests, and the lack of refugia for nat-
ural enemies, particularly parasitoids (Hoelmer 1995). Augmentation biological con-
trol shows potential for overcoming the difficulties of working in these ephemeral
cropping systems. Early season releases of Eretmocerus spp., integrated with the use
of selective insecticides, such as imidacloprid can provide season long control ofB. ar-
gentifolli without the need for late season applications of broadspectrum insecticides
(Simmons et al. 1997, Ciomperlik et al. 1997).
The high cost of producing and releasing natural enemies often limits the use of
augmentative biological control. Although several field trials have shown that aug-
mentative releases of natural enemies can suppress pests in field and orchard sys-
tems, the cost of application precludes their use (Pickett & Bugg 1998). Typically
augmentative biological control is used in high value crops with a large budget for
production costs, i.e. strawberries, glasshouse crops (Ravensberg 1992, Trumble &

















Florida Entomologist 82(4)


December, 1999


Morse 1993). Cucurbit crops such as spring cantaloupe melons also fit these criteria
making it economically feasible to use augmentative biological control. In all of these
crops, increasing the efficiency of field delivery systems can reduce application costs.
This is especially critical to short season annual crops where the window of time for
effective pest management is short in contrast to perennial systems.
It has been demonstrated that releases of the newly imported exotic Eretmocerus
spp. can suppress B. argentifolii populations in spring cantaloupe melon crops (Sim-
mons et al. 1997, Ciomperlik et al. 1997). In these tests hand releases have been used
to augment parasitoid populations. A method is needed which allows for efficient
early season mass release of parasitoids in cucurbit crops. Herein we propose a novel
approach for augmenting Eretmocerus that can increase the efficiency of delivery over
hand releases.
Methods were developed and tested using greenhouse grown seedling transplants
inoculated with parasitoids, called "banker plants," specifically for augmenting para-
sitoids in annual cucurbit crops, and with possible application in other transplanted
vegetable crops such as tomatoes and cole crops. The term banker plant was used by
Vet et al. (1980) to describe the use of parasitoid inoculated tomato plants for release
of Encarsia formosa Gahan to control Trialeurodes vaporarium (Westwood) in green-
houses. Similarly, Bennison (1992) described the use of banker plants to augment
aphid parasitoids in greenhouse cucumbers. We have extended the use of the term
"banker plants" to describe parasitoid inoculated seedling transplants for use in field
settings.
Banker plants have many advantages for field release of natural enemies in an-
nual crops such as spring melons. Large numbers of transplants can be inoculated in
the greenhouse, capitalizing on the inherent distribution system of transplant nurs-
eries, and moved to many widely dispersed fields. Transplanting is mechanized which
allows for efficient, large scale planting of banker and regular transplants in field
crops. Parasitoids transported to the field by banker plants are immatures on the un-
derside of the leaf which are not as susceptible to mortality factors such as rain, heat,
wind, etc., as are adults or pupae released on clipped leaf material. Banker plants also
aid in the dispersal of parasitoids within a field. As the transplants are planted,
banker plants can be evenly spaced with regular seedlings to provide uniform distri-
bution and emergence of parasitoids across the field. This should increase searching
efficiency of parasitoids since they can search a smaller area before finding a host.
This is critical during early season when pests are highly clumped in distribution and
difficult to find. Lastly, banker plants allow for early season release of parasitoids in
precise synchrony with the establishment of the crop and with timing of the insecti-
cide imidacloprid, Admire".
A series of field and lab experiments were conducted in 1996, 1997 and 1998 to de-
velop methods for producing banker plants. Plant screening determined the suitabil-
ity of varieties for use as banker plants. We predicted that some varieties would not
be suitable for use as banker plants because of their susceptibility to B. argentifolii.
Ten varieties were selected Riley's (1995) report, Melon cultivar response to Bemisia.
The selections we made represented the most popular varieties in terms of acres
planted and/or varieties which were listed as susceptible to B. argentifolii. Lab tests
measured the impact of imidacloprid on developing parasitoids. This insecticide is
systemic, widely used by melon producers, and is considered critical to season long
whitefly control (Castle et al. 1996). Finally, field trials were conducted in spring can-
taloupe and fall watermelon plantings to quantify the numbers of parasitoids pro-
duced using banker plants. Eretmocerus hayati Rose & Zolnerowich (accession #
M95012) from Multan, Pakistan, was used in all the tests based on its performance in

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 535

previous laboratory and field evaluations (Goolsby et al. 1998). Our target release
rate in cantaloupe was 23,000 per acre or one parasitoid per plant. This release rate
was based on field studies conducted from 1993 to 1996 (Ciomperlik & Goolsby, un-
published data). Field tests during the Spring of 1997 with spring melons were con-
ducted on the research farm at the Mission Biological Control Center, Moore Airbase,
Mission, TX. Later trials were conducted with growers to determine the feasibility of
large-scale transplanting of banker plants in commercial agriculture. In all of these
trials we determined both the numbers of parasitoids produced per banker plant and
release rate per acre. Efficacy of the augmentation program is discussed elsewhere.


MATERIALS AND METHODS

Banker Plant Inoculation Methods

Cantaloupe and watermelon transplants used in the tests were grown in styro-
foam flats with 128 cells 3.8 cm in diameter with a depth of 7.62 cm in a greenhouse
held at 27 + 2C with a natural 14:10 L:D photoperiod. Flats were covered with an or-
ganza material shroud and were inoculated with adult B. argentifolii when the first
true leaves were 1.8 cm across at the widest portion. Whitefly adults were collected
from eggplants using a high volume, low velocity vacuum and transferred into clear
one-gallon plastic containers for counting. The numbers of adult whitefly were esti-
mated by counting the number of settled adults in ten separate 1 cm2 discs located on
the sides of the container. The average number of adults per cm2 were multiplied by
the surface area of the container to obtain the total estimated number of whitefly. Ap-
proximately 5000 adult whitefly were released per shrouded flat. Subsequent egg den-
sities were determined by counting the number of eggs on a 1 cm2 disc on the first true
leaf of seedlings selected randomly from each flat.
Four hundred and fifty adult E. hayati, reared from B. argentifolii on eggplant,
aged 24-48 h old, were released in each production flat. Parasitoids were collected
from emergence cages in petri plates and had a male to female sex ratio of 40:60. Each
plate was provisioned with a streak of honey and the parasitoids were held at 15C
until release. Parasitoids were released onto the plants when the majority of the
whitefly eggs had hatched and the crawlers became settled first instars.
Counts to estimate the mean number of E. hayati per transplant were made 20
days after inoculation or when the majority of parasitoids had emerged. Counts were
conducted in the laboratory using dissecting microscopes to determine the status of
every individual on the 1 cm2 leaf disc being recorded on a data sheet. Categories for
the status of individual determinations were as follows: eggs; small nymphs (1st, 2nd,
and 3rd instar), large nymphs (4th instar), (live, dead); emerged whitefly; parasitoid
immatures; parasitoid mummies. Large nymphs were used to calculate percent par-
asitism because we could clearly determine if they were parasitized or not.

Cantaloupe Variety Screening

We used choice tests to evaluate the effect of cantaloupe variety on fecundity of
SLWF and parasitoids. Ten varieties were tested: 'Primo', 'Explorer' (Rogers Seed),
'Cruiser' (Harris-Moran Seed), 'Marco Polo', 'Copa de Oro', 'Mission', 'Pacstart' (As-
grow Vegetable Seeds), 'Mainpak' (Sun Seeds), and 'Laredo', and 'Durango' (Peto
Seed). Ten plants of each variety were planted in each of 4 flats. Cantaloupe seeds
were planted at the same time and maintained in a greenhouse at 27C with a natural

















Florida Entomologist 82(4)


December, 1999


15:9 L:D photoperiod. Cages consisted of 100 seedlings in styrofoam transplant flats
surrounded by an aluminum frame (38 x 80 x 40 cm), covered with organza. Seedlings
were inoculated with adult whitefly and parasitoids using the methods described
above. Twenty days after introduction of the parasitoids the leaf samples were re-
moved and nymphal SLWF were analyzed with a stereo microscope to determine in-
cidence of parasitism. Percent parasitism was calculated as the number of parasitized
4th instar nymphs and parasitoid mummies divided by the total number of parasit-
ized and non-parasitized nymphs.
Statistical comparisons were analyzed using ANOVA and means were separated
by the Tukey Studentized range test (SAS Institute 1998). The following parameters
were compared: 1) total numbers of SLWF; 2) total numbers of parasitoids produced;
and 3) percent parasitism. Percent parasitism data was arcsin transformed for the
analysis.


Toxicity of Imidacloprid to Parasitoids

The impact of imidacloprid on immature E. hayati was measured. Eight flats of
seedling plants were grown in a greenhouse at 32 + 5C under the natural 16:8 L:D re-
gime which occurs during early summer. Cantaloupes var.'Primo' were shrouded with
organza and infested with whitefly and parasitoids using the same methods described
above. Imidacloprid, Admire 2F was applied in a sequence to selected flats on days 0,
2, 4, 6, 8, 10, and 13 following release of the parasitoids. An eighth flat was not treated
with imidacloprid and served as a control. Each flat was treated using a micro pipet
with 0.53 mls imidacloprid per 2 gals of water, which is equivalent to the dose the same
number of plants would receive in the field (pers. comm., S. Fraser, Miles, Inc.).
To assess the impact of imidacloprid on parasitoid immatures, the first true leaf
from each plant was sampled 20 days after inoculation to allow live parasitoids to
emerge. Categories for the status of individual determinations were as follows: small
nymphs (1st, 2nd, and 3rd instar), large nymphs (4th instar), (live, dead); parasitoids
(live, dead) and emerged whitefly. Unemerged parasitoids were considered to be dead.


Field Estimates of Release Rates

Banker plants used for transplanting were grown in a greenhouse and inoculated
using the methods described above. Transplanting was conducted 2-6 after inoculation
of whitefly with parasitoids, and depended on rainfall and grower schedules. Growers
applied midacloprid by a drip system, in all of the tests, between one and three weeks
after transplanting. No other insecticides were applied to the crop, however selected
fungicides were used later in the season after emergence of the parasitoids.
To estimate the number of parasitoid progeny produced per banker plant, counts
were made from a randomly collected field sample of banker plants. Similar emer-
gence studies were conducted from a random sample of three banker plants from each
flat held in the greenhouse. We sampled the first true leaf of the banker plants to es-
timate the numbers of parasitoids produced per plant. In some cases, we also counted
the second true leaf if parasitoid pupae or mummies were observed.
To compare fruit yields between banker and regular transplants we counted the
total number of marketable cantaloupes on 30 vines each respectively. We considered
a marketable melon to be any size between #9 and #15 (Miller, 1997). Yield counts
were conducted one day before the first initial harvest of the field. The numbers of
fruit per vine between banker and regular transplants were analyzed by t-test (SAS
Institute 1998).

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 537

Cantaloupe var 'Primo' was selected for both 1997 and 1998 field trials based on
earlier screening work. The first field evaluation of banker plants was conducted in
April of 1997 at the Biological Control Demonstration Farm at Moore Airbase. Banker
plants were mechanically transplanted simultaneously with the regular transplants
at a ratio of 1:10, banker to regular transplants. The second cantaloupe banker plant
trial was transplanted at a ratio of 1:30 on Feb. 17, 1998 into a commercial field in San
Juan, TX which was direct seeded on Jan. 20, 1998. In the Fall 1997, watermelon tri-
als were conducted on a commercial farm in Mission, TX. At each location one half of
the transplants were a triploid seedless watermelon var. Abbott & Cobb # 5441, in a
mix of every other transplant with a diploid watermelon var.'Royal Sweet'. We inoc-
ulated 1 out of 15 diploid watermelon transplants, which resulted in a ratio of 1:30
banker plants to regular transplants. The field in Mission, TX was hand transplanted
on Aug. 1, 1997.

RESULTS AND DISCUSSION

Cantaloupe Variety Evaluation

Varieties Copa de Oro and Mission had significantly higher densities of large
nymphs than the other varieties tested (F = 4.46; df = 9, 403; P < .0001) (Fig. 1). Sim-
mons and McCreight (1996) also found differences in whitefly preference for selected
cantaloupe germplasm. We compared nymphal densities which may be an indicator of
survival of nymphs after oviposition, more than an indicator of adult SLWF prefer-
ence. However, mortality of the 1st instar crawlers was very low (<5%), based on the
status of individual counts, which suggests that nymphal densities corresponded with
adult oviposition rates. Copa de Oro, Mission, and Primo produced significantly more
parasitoids than the other varieties (F = 4.08; df= 9, 403; P < 0.0001). Primo produced
equivalent numbers of parasitoids to Asgrow and Mission, even though the latter two
varieties had significantly higher SLWF densities. This suggests that parasitoids may
show a preference for Primo. Primo also had the highest mean level of parasitism, but
it was not significantly different from the other varieties (F = 1.06; 9, 403; P > 0.3948).
Based on these results, the cultivar Primo was selected for further development of the
banker plant delivery system.
These tests indicate there may be differences between cantaloupe varieties that
could influence densities of whitefly, and subsequently the number of parasitoids that
can be produced on banker plants. It appears that Primo is a suitable variety for test-
ing the banker plant delivery system. However, other varieties could likely be used as
banker plants if whitefly densities were manipulated during infestation of the seed-
lings. Fortuitously, Primo is also one of the most commonly planted cantaloupe vari-
eties in the Lower Rio Grande Valley of Texas.

Toxicity of Imidacloprid to Parasitoids

The effect of imidacloprid on the mean number of parasitoids produced was signif-
icant for treatment date (F = 17.91; df = 7, 205; P < .0001), (Fig. 2). It appears that im-
idacloprid caused high levels of mortality in developing parasitoid immatures up to
six days after inoculation. By day 13, there was no significant difference in numbers
of parasitoids produced as compared to the control.
The method by which the parasitoid larvae escaped the effect of imidacloprid is not
known. One explanation may be that by day six the parasitoid larvae had matured to
the point where it had killed the host. After death, the whitefly ceases to uptake plant




















Florida Entomologist 82(4)


December, 1999


ilij '-" b A bc bb


i i itii :
+ I, 3 b3"b .i h :,o


Si i


6 0 a

50 ab

40 ab

bc bc
30 k. o




10 ti
100 -




MO.1


a
a
aa


1 all-^,_ a'4



oo. ,+" ;ra+! ,. o,! BE+. :
.4 ** 4 -/ I


Fig. 1. Summary of cantaloupe variety evaluation. Numbers of B. argentifolii and
parasitoids are per leaf (~ 25 cm2). Bars with the same letter are not significantly dif-
ferent (P = 0.05).


180

160

140
E
S120

. 100
6 80
d
S 60

s 40

20

0


(0
V

I
C
C-
a
d
c
C
Ia
a,


90

Ss80
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I 70
S. 60


C 40

S30

S20
10

0

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 539

100 ---
U) a
90 a
S80-


60 B3
o a I
50




20
10 d d d


Day 0 Day 2 Day 4 Day 6 Day 8 Day 10 Day 13 Control

Fig. 2. Mean number ofE. hayati adults produced per leaf(~ 25 cm2) after applica-
tion of imidacloprid insecticide. Bars represent the day banker plants were treated
with imidacloprid following inoculation with parasitoids on Day 0. Bars followed by
the same letter are not significantly different (P = 0.05) in total number of parasitoids
produced.


fluids containing the imidacloprid. For practical purposes, if applications of imidaclo-
prid could be delayed for one week after transplanting, or if banker plants could be
planted one week after they are inoculated with parasitoids, the impact on developing
parasitoids would be minimized. Timing of the imidacloprid application should be
temperature dependent. If cool weather delays development of the whitefly imma-
tures and parasitoids, the insecticide application may need to be delayed.


Field Production Estimates

1997 Cantaloupe. Numbers of whitefly and parasitoids used to inoculate the trans-
plants are listed in Table 1. The egg density was estimated to be 88 per cm2. Overall
whitefly density appeared to have had an adverse effect on plant health due to early
senescence of leaves. Egg and nymphal densities this high are routine in mass rearing
procedures using mature eggplant and hibiscus plants (Goolsby, unpublished data).
However, young cantaloupe seedlings may not be able to tolerate this level of infesta-
tion. Despite some early senescence of the parasitoid bearing 1st true leaves, parasi-
toid production met the target release rate (Table 2). Fecundity per female was high
with a 26.7 fold increase across 40 flats of banker plants. In comparison, a 12 fold in-
crease is typical in other outdoor rearing systems (Goolsby, unpublished data). The
higher fecundity may be due to the confinement of the parasitoids with the whitefly
infested transplants in the shroud cages along with moderate temperature and hu-
midity found in the greenhouse environment. Field estimates of the number of para-
sitoids produced per banker plant was hampered by persistent rains that drenched
the crop during the month of March. Hence, we were unable to sample the banker
plants in the field to determine the release rate. We estimated the release rate based
on subsample of banker plants which we held in the greenhouse to be approximately
three times the target release rate of 23,000 per acre (Table 3). We determined from
these trials that the ratio of banker plants per acre could be reduced to 1:30 while still
producing the target release rate.

















Florida Entomologist 82(4)


December, 1999


TABLE 1. WHITEFLY AND PARASITOID INPUTS PER BANKER FLAT.

Cantaloupe Cantaloupe Watermelon
Spring 97 Spring 98 Fall 97

Mean no. of adult 6239 + 302 4633 + 342 5335 + 177
whitefly released + SE
Mean egg density + SE 85.6 + 8.8 43.9 + 6.5 43.6 + 4.9
Mean no. of parasitoid
females released + SE 246.4 + 18.1 523.7 + 13.7 296.6 + 26.2
Sex ratio of parental 32:64 43:57 n/a
material M:F



1998 Cantaloupe. Egg density was determined to be 43.9 per cm2. This appears to
be nearly the optimum density for health of the banker plant as compared to 88 per
cm2 recorded in the earlier 1997 trial. At this egg density, very few of the first true
leaves senesced, which resulted in a higher mean number of inoculating parasitoids
produced per banker plant (Table 2). Lower densities of nymphs and higher numbers
of parasitoid females resulted in higher levels of parasitism as compared to the 1997
trial. Fecundity per female was also higher at 38.6 than the 97 trial (Table 2). Esti-
mates of the mean number of parasitoid progeny produced per banker plant were
102.1 and 32.8 from the greenhouse and field, respectively. The actual number of
progeny produced per plant is likely to fall between these two estimates. Field counts
underestimate progeny production due to the fact that mummies may fall off after
emergence of the parasitoid (Table 2). Other workers have also found that parasitoid
mummies are sometimes dislodged from the plant leaf (Naranjo, pers. comm.). The
mean number of parasitoids produced by pooling both estimates is 67.5 per banker
plant which translates to 29,970 per acre (Table 3). This rate is slightly higher than
the target rate of 23,000 per acre. Based on these estimates, the number of banker


TABLE 2. PRODUCTION ESTIMATES OF BANKER PLANT PRODUCTION.

Cantaloupe Cantaloupe Watermelon
Spring 97 Spring 98 Fall 97

Greenhouse Estimate
Parasitoids per banker
plant + SE 94.6 + 17.9 102.1 + 14.5 94.6 + 16.7
Mean percent parasitism 49.4% 57.3% 56.0%
Mean fecundity
per female 26.7 38.6 40.8

Field Estimate
Parasitoids per banker
plant + SE n/a 32.8 + 5.8 9.3 + 7.2
Average percent
parasitism n/a 41.8% 71.8%
Mean fecundity n/a 14.6 4
per female

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 541

TABLE 3. FIELD RELEASE RATE BASED ON POOLED GREENHOUSE AND FIELD ESTIMATES.

Cantaloupe Cantaloupe Watermelon
Spring 97 Spring 98 Fall 97

No. of banker plants: 1:10 1:30 1:0
regular transplants
No. of banker plants
per acre 906 444 80
Estimated no. released
per acre 68,9461 29,970 4,156
Target release rate 23,000 20,000 1,100
No. of acres in test 5 45 45

'Rate based on greenhouse estimate alone.



plants per acre could be lowered for several reasons. Spring cantaloupe fields in the
LRGV are usually planted in January when whitefly levels arevery low (Riley & Ci-
omperlik 1998). Earlier banker plant trials were conducted with cantaloupes planted
in March at ratios of 1:10. Banker to regular transplant ratios of 1:50 or 1:100 may be
suitable for early planted spring crops when whitefly levels are low and augmented
parasitoids have additional time to build their populations.
1997 Watermelons. Numbers of whitefly and parasitoids used to inoculate the wa-
termelon transplants are listed in Table 1. The egg density was determined to be 43.6
per cm2. This appears to be nearly the appropriate density for watermelons and can-
taloupe banker plants. At this whitefly density, plants maintain good vigor through-
out the seedling growth stage and in the field as transplants. Percent parasitism
ranged from 56% in samples of greenhouse banker plants to 71.8% from the field col-
lected material. This level of parasitism in watermelon is slightly higher than experi-
enced in the cantaloupe trials, even though lower numbers of parasitoid females were
used in their inoculation (Table 1). Similarly, the mean number of parasitoid progeny
produced per female was higher in the watermelon transplants (40.8) as compared
with cantaloupes (38.6). The higher level of parasitism and mean progeny production
per female may be in part due to differences between the watermelon and cantaloupe
transplants. Watermelon transplants are typically grown to about twice the size of the
cantaloupe before transplanting. The larger transplant has two true leaves available
for infestation with whitefly. Mutual interference of searching females may be mini-
mized by the larger leaf surface area of the watermelon seedling.
Progeny production estimates of greenhouse and field grown banker plants were
94.6 and 9.3 respectively (Table 2). The large difference between the two estimates is
likely due to the harsh field conditions experienced during August in the LRGV. When
the field was transplanted, water stress and strong winds adversely affected the
young seedlings. Some of the developing parasitoids may not have survived, and
many of the parasitoid mummies may have been dislodged from the leaf. Pooling the
two estimates leads to a field release rate of 4156 parasitoids per acre (Table 3). Given
the high rate of whitefly migration into the young watermelons from surrounding ar-
eas of defoliated cotton, the current banker to regular transplant ratio in watermelons
seemed appropriate for these growing conditions. Inoculating 2 diploid transplants
out of 15 would increase the banker plant ratio to 1:15. Using the higher banker plant
to transplant ratio may be advisable during periods of heavy whitefly migration.

















Florida Entomologist 82(4)


December, 1999


This research demonstrates that the use of banker plants is a reliable method for
augmenting Eretmocerus parasitoids in both cantaloupe and watermelon crops. Vari-
etal differences in cantaloupes seemed to affect oviposition by Bemisia and rates of
parasitism by E. hayati. However, differences were not so great as to exclude the use
of a particular variety for use as a banker plant. Manipulation of adult whitefly and
parasitoid numbers should overcome any varietal restraints. We recommend the
same species of plant and variety be used for the banker plants as the field crop. Irri-
gation timing, weed control practices, fertility, etc., will be directed towards the crop.
By using the same variety as the crop, unpredicted effects of different varieties or
plant species can be avoided. In addition, the banker plant will produce a normal
yield, thus offsetting the cost of the plant in using parasitoid inoculated transplants.
In our tests, cantaloupe melon production was not significantly different between reg-
ular and banker plant vines (Table 4).
Laboratory studies document the potential for integrating imidacloprid with
banker plants and augmentation strategies for management of SLWF. Our tests show
that parasitoid immatures in the later stages of development were not effected by im-
idacloprid. Use of imidacloprid is standard practice in most subtropical growing areas
of the U.S. and worldwide. Combining the use of imidacloprid, a density independent
mortality factor, combined with parasitoids, a density dependent factor, may be syn-
ergistic in providing better control of B. argentifolii than would occur if the two factors
were used separately. Eretmocerus hayati is capable of finding low density whitefly
immatures that are typical after imidacloprid applications. This strategy may provide
season long control of Bemisia, thus avoiding late season applications of broadspec-
trum insecticides, or unlabelled applications of imidacloprid which could increase the
likelihood of resistance.
From our work using banker plants in direct seeded melon crops, another alterna-
tive for timing of imidacloprid became apparent. Imidacloprid could be applied to the
direct seeded crop at planting providing full protection to the seedlings as they
emerge. The banker plants could be held in the greenhouse until parasitoids have
reached the late larval or early pupal stage and then be transplanted. If banker plants
were held in the greenhouse for an additional week at 27C, parasitoids on the trans-
plants should not be affected by imidacloprid.
The production and use of banker plants for augmentation does not require any
additional technological hurdles for implementation. Production of sufficient num-
bers of parasitoids for inoculation of banker plants for many thousand acres of cucur-
bits is feasible. Growers have the option of using banker plants with their regular
transplants or in direct seeded crops, both of which have been demonstrated success-
fully in our field trials. Additional benefits from these augmentation programs may be



TABLE 4. COMPARISON OF CANTALOUPE FRUIT YIELDS BETWEEN BANKER PLANTS AND
REGULAR TRANSPLANTS.

Mean no. + SE Fruits

Year Regular Plants Banker Plants

1997 1.5 0.2" 1.4 0.1"
1998 1.1 0.1" 0.8 0.1"

Means within rows followed by the same letter are not significantly different (P = 0.05).

















Goolsby & Ciomperlik: Parasitoid Inoculated Transplants 543

derived if the exotic parasitoid is able to migrate in sufficient numbers to surrounding
summer crops such as cotton, soybean, and alfalfa, or to fall crops such as cucumber
and cole crops. Whitefly may be regulated at lower levels if sufficient numbers of par-
asitoids colonize the summer and fall crops. Studies are needed to quantify the dis-
persal capabilities of E. hayati, from fields where it has been augmented, to
surrounding fields. Banker plant delivery methods could be used to implement area-
wide biological control programs directed against SLWF. Area wide releases of para-
sitoids via banker plants could potentially moderate whitefly levels at a regional level.
Lastly, more detailed studies evaluating the efficacy of augmentation using banker
plants as compared to other release methods are needed.
Parasitoid inoculated seedling banker plants represent a novel method for field re-
lease of parasitoids in field settings. Banker plant methods could be used to augment
many different parasitoid species against a variety of pests. For instance, parasitoids
could be augmented via cabbage and broccoli banker plants for control of SLWF. Like-
wise, parasitoids of Plutella xylostella (L.), the diamondback moth, could be aug-
mented on broccoli using the banker plant delivery methods. In many cases, early
season augmentation of parasitoids has already shown to be effective for controlling
a variety of insect and mite pests (Parker & Pinnell 1972, Biever & Chauvin 1992,
Hoffman & Frodsham 1993). Parasitoid inoculated banker plant methods could en-
able other augmentation programs and extend the use of biological control in annual
cropping systems.


ACKNOWLEDGMENTS

We appreciate the help of the following people Albino Chavarria and the produc-
tion personnel at the Mission Plant Protection Center, Jim Carson, Speedling Inc.,
Growers: Mike Helle, Roel Basaldua, and Fred Schuster; Field Technicians: Mateo
Hernandez, Johnny Rodriguez, and Danny Martinez; and Lloyd Wendel (Center Di-
rector) for support of the research. We would also like to thank Charlie Pickett, Benjie
Legaspi, and Alvin Simmons for their thoughtful review of the manuscript.


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J. Econ. Entomol. 86:879-885.
VET, L. E. M., J. C. VAN LENTEREN, AND J. WOETS. 1980. The parasite-host relation-
ship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes
uaporariorum (Homoptera: Aleyrodidae). IX. A review of the biological control
of the greenhouse whitefly with suggestions for future research. Z.ang. Ent. 90:
26-51.
















Florida Entomologist 82(4)


December, 1999


MORPHOLOGY AND DISTRIBUTION OF THE SENSE ORGANS
ON THE ANTENNAE OF COPITARSIA CONSUETA
(LEPIDOPTERA: NOCTUIDAE)

VICTOR R. CASTREJON-GOMEZ', JORGE VALDEZ-CARRASCO2,
JUAN CIBRIAN-TOVAR2, MARIO CAMINO-LAVIN' AND RODOLFO OSORIO 0.2
1Departamento de Interacciones Bioquimicas Planta-Insecto, Centro de Desarrollo
de Products Bi6ticos del Instituto Polit6cnico Nacional, Apartado Postal 24,
Carretera Yautepec, Jojutla Km. 8.5, Yautepec, Morelos, MEXICO

2Instituto de Fitosanidad, Colegio de Postgraduados, 56230 Montecillo,
Estado de M6xico, MEXICO


ABSTRACT

Five types of sensilla were found on the antennae of adult Copitarsia consueta
(Walker) (Lepidoptera: Noctuidae) by scanning electron microscopy and light micros-
copy. Those sensilla were trichoidea, coeloconica, styloconica, basiconica and squami-
formia. Two types of sexually dimorphic sensilla trichodea were found; type I is in the
border of the sensory field of the flagellar segments and present only on male anten-
nae. This suggests that the sensillum may contain the receptor sites for the female sex
pheromone. Type II is located within the ventro-medial sensillar field where it is ar-
ranged without apparent pattern. Six types of sensilla chaetica were found around
antennal segments, and were particularly abundant on the apical antennal segment.
One sensillum styloconicum was identified per segment, except for the apical seg-
ment, where it varies in number. Each sensillum consists of a base, a stalk and a cone.
Each flagellar segment bears several sensilla coeloconica on the ventral surface, situ-
ated on or near distal edge. Each sensillum consists of a depression surrounded by 15
to 17 "teeth" and one peg. Two types of sensilla basiconica were identified, type I is
more curved and broader than type II.

Key Words: antennal morphology, sensilla types, sexual dimorphism


RESUME

Se reconocieron cinco tipos de s6nsulos en la antena de la palomilla Copitarsia con-
sueta (Walker) (Lepidoptera: Noctuidae) por medio de microscopia electr6nica de ba-
rrido y microscopia de luz. Dos tipos de s6nsulos tricoideos fueron observados; el tipo
I se localiz6 en las parties laterales del area sensorial y estuvo present s6lo en la an-
tena del macho, lo cual sugiere que este tipo de s6nsulo puede ser el receptor de la fe-
romona sexual de la hembra. El tipo II se localiz6 en la parte ventral y no tuvo ningun
patron de distribuci6n. Ademas se observaron otros seis s6nsulos queticos alrededor
de cada segment, except en el segment apical donde el numero fue mayor. Se iden-
tific6 un solo s6nsulo estiloc6nico por segment ubicado en la parte media distal, pero
en el segment terminal el numero vari6, este s6nsulo consta de una base, un peciolo
y un cono. Varios s6nsulos celoc6nicos se identificaron en la superficie ventral, se ob-
servaron de la parte media a la distal del segment antenal, cada uno estuvo formado
de una depresi6n rodeada por 15 a 17 "dientes o espinas" y una "estaquilla". Dos tipos
de s6nsulos basic6nicos fueron identificados; el tipo I fue mas curvado en la parte final
y mas ancho en la base que el tipo II.

















Castrejon et al.: Sense Organs of Copitarsia consueta


Copitarsia consueta infests various crops of economic importance throughout most
of the Americas (Angulo & Weigert 1975). In Bolivia it is considered a pest of potatoes,
(Munro, 1968), and in Mexico a pest of cabbage (Monge, 1984).
Rojas et al. (1995) identified the sites of sex pheromone production in C. consueta
using morphological and histological evidence. Typically, the detection of the sexual
pheromone in noctuid moths is by olfactory neurons in sensilla on the male antenna
(Lavoie & McNeil 1987). A knowledge of the structure and distribution of sensory sen-
silla of the male is an important precursor to electrophysiological and behavioral
studies.
In this paper we describe the sensory structures of male and female C. consueta
antennae, as seen through scanning electron and light microscopes.

MATERIALS AND METHODS

The insects were obtained from a colony raised on an artificial diet (Cibrian & Sug-
imoto 1992) in a laboratory at Colegio de Postgraduados, Estado de M6xico at 25 +
3C, 60 + 5% RH and a photoperiod of 14:10 hr L:D.

Scanning Electron Microscopy (SEM)

The antennae of 15 males and 15 females were separately placed in a solution of
70% ethanol and 2% formaldehyde for 24 hours. They were then dehydrated in 80%,
90%, and 100% ethanol for 8 hr each. Afterwards, they were dried at the critical point
and finally gold coated (70 nm) for observation with a JEOL 35-C microscope at 5 and
10 kV (Wall 1978, Valdez 1991). The average length and basal diameter of the external
part of each sensillum was calculated through 15 measurements taken from photomi-
crographs (Faucheux 1991).

Light Microscopy (LM)

The antennae of both sexes were macerated in 10% KOH at 80C until they cleared
(approximately 30 minutes). They were washed with distilled water of equal temper-
ature and for the same amount of time. The scales were removed with a 60 Hz ultra-
sonic cleaner for one minute, and the antennae were then dehydrated in 70% and
100% alcohol for 30 and 60 minutes respectively. Finally, they were cleared with xylol
and mounted in Canada balsam. The observations were made with a Meiji (40x) mi-
croscope. The sensilla were counted on each flagellar segment on the antennae of 10
males and 30 females (Faucheux 1991).

RESULTS

General Morphology of the Antennae

The antenna of C. consueta is filiform and segmented, and the flagellum is spindle-
shaped. Each antenna consists of two basal segments: the scape and the pedicel. On
the antennae's dorsal surface are "Bohm" bristles. The number of flagellar segments
is similar in males and females. A typical antennal segment is cylindrical and divided
into two main areas. The dorsal surface has two rows of scales; the second row over-
laps the first row of the following segment. The only obvious type of dorsal sensillum
is of the squamiform type (Fig. 1). The ventral surface possesses most of the sensilla,
and these are of various types (Fig. 2).

















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December, 1999


External Morphology and Distribution of Sensilla

The antenna of the male is approximately 11.22 mm long + 0.08 (SEM). In the fe-
male the antenna measures 11.37 + 0.09 mm. The number of segments is slightly
greater in the flagellum of the female (77.3 0.57) than in the male (75.6 + 0.45) (av-
erage of 30 antennae, 15 insects in each case) (Table 1). The flagellar segments dimin-
ish in length and diameter from the base to the apex of the antenna and have the
same general organization and pattern of sensory structures. The segments are larger
in the male than in the female (Table 1). There are 5 types of sensilla on the flagellum:
trichoid, basiconic, coeloconic, styloconic and squamiform sensilla.
Males and females have the same types of sensilla on the ventral surface of flagel-
lar segments, except for the lateral chemoreceptive trichoid sensilla, which are
present only in the male.
The chemoreceptive trichoid sensilla are the most numerous type. They can be di-
vided into two groups according to their external structure and location. Type I,
present only on the antenna of the male are the longest (Table 2). They are set in 4 or
5 parallel rows on the sides of the ventral sensory area of the proximal and median
segments (Fig. 3). The number of sensilla decrease from 278 at the base of the flagel-
lum (average of the first 5 segments of 5 antennae), to fewer than 100 (average of the
segments 51 to 55 of 5 antennae) and disappear between segments 66 and 68. The to-
tal number of these sensilla was estimated to be 2814 + 144.6 (Table 3).
Type II sensilla are localized on the ventral surface of each segment and are
shorter than type I sensilla. They are not arranged in rows (Fig. 2), and are larger in
the male than in the female (Table 2). Some of these sensilla are more curved than
others (Fig. 4), but the differences are too small to reliably characterize two forms. The
total number of these sensilla was larger in the male than in the female (Table 3).
Each segment the male and female antennae bear six mechanoreceptive sensilla
chaetica, except the apical segment which has more than six (Fig. 5). Each sensillum
is straight, wide at the basal part and slightly curved at the distal part, blunt
(rounded), and without a pore. These sensilla can be divided into two groups according
to their length. Long sensilla chaetica, found on the superior dorsal surface (2) and
lateroventrally (2) (Fig. 5), are larger in the male than in the female (Table 2). The to-
tal number of these sensilla was calculated as 302.4 + 1.82 in the male, and 309.2 +
2.31 in the female (Table 3). Contrasting with this, are the short sensilla chaetica, lo-
calized on the medio-ventral surface (2) (Fig. 5). They are shorter and narrower in the
male (65.17 3.18 in length and 3.44 0.35 in width at the base) than in the female
(67.10 4.61 in length and 3.55 0.01 in width) (Table 2). The total number of short
sensilla was estimated to be 151.13 + 0.93 in the male and 154.53 + 1.13 in the female
(Table 3).
In both males and females there is a single styloconic sensillum (from the third
segment onward) in the middle part of the distal edge of each segment (Fig. 6), how-
ever, their number varies on the terminal segment. The average length of the com-
plete structure (stalk and cone) in males and females is 2.58 0.04 and 2.20 0.04
respectively (Table 2). On the antenna of the male there are approximately 72.6 + 0.45
sensilla and on the female antenna 74.3 + 0.58 (Table 3). The styloconic sensillum in
C. consueta has a reticulated base, a relatively smooth (plain) petiole and a conic ex-
tremity; some of them have a double or triple apical structure (Fig. 6).
On each flagellar segment there are several coeloconic sensilla on the ventral sur-
face (Fig. 7); they are situated mainly from the middle to the distal portion of the seg-
ment. Each sensillum consists of a depression surrounded by 15 to 17 cuticular
"spines" and a porous peg with longitudinal striations on its surface, arising from the
center of the depression (Fig. 7). The diameter of the coeloconic sensilla varies from
















Castrejon et al.: Sense Organs of Copitarsia consueta


Fig. 1. Dorsal surface of a C. consueta male antenna. Sq = sensillum squamifor-
mium. S = scales; Lt = lateral trichoid sensilla. Bar = 100 Pm. Fig. 2. Ventral surface
of a female antenna. Vt = ventral trichoid sensilla; Arrows indicate limits of one seg-
ment. Bar = 10 pm. Fig. 3. Laterodorsal surface of a male antenna. Lt = lateral tri-
choid sensilla. Bar = 100 pm. Fig. 4. Types of ventral trichoid sensilla. St = straight;
Cu = curved; Sty = sensillum styloconicum. Bar= 10 pm.

















Florida Entomologist 82(4)


December, 1999


TABLE 1. THE TOTAL LENGTH AND NUMBER OF SEGMENTS (X SEM) IN THE ANTENNAL
FLAGELLUM OF MALE AND FEMALE COPITARSIA CONSUETA (WALKER).

Length of the Number of Length of the Width of the
Sex antennae (Pm) segments segments (pm) segments (pm)

Male 11.22 + 0.08* 75.6 + 0.45* 155.72 + 12.4a 139 + 3.2a
(10.4-12) (71-80) (89.65-13.79) (117.24-158.62)
Female 11.37 + 0.09* 77.3 + 0.57* 150.86 + 5.11a 130.06 + 2.56a
(10.2-12) (72-83) (120.68-175.86) (120.68-151.72)

*n = 30 antennae. On = 15 segments (range in parentheses).


10.44 0.45 in the male to 11.13 + 0.55 in the female (Table 2). The number of sensilla
per insect is similar in males and females, 422.9 17.18 in males and 419.9 + 2.97 in
females (Table 3). There are fewer of them at the base (<3 per segment). The number
increases in the central part (- 8) and diminishes again at the point (- 4).
Two types of basiconic sensilla, different in shape, can be observed on the ventral
part of the antenna of C. consueta (Fig. 8). They are smaller than all but the coeloconic
sensilla. Type I is more curved at the terminal part, and the base is wider than in type
II, which has the shape of a small stake; both are rounded at the apex. There are ap-
proximately 2 sensilla of each type per segment.
The squamiform sensilla, positioned on the dorsal part of the antenna among the
scales, are shorter and finer than the scales (Fig. 1).

DISCUSSION

The general structure of the antenna of C. consueta is similar to that in other noctu-
ids: Trichoplusia ni (Hubner), Helicoverpa zea (Boddie), Spodoptera ornithogalli
(Guene6), Spodoptera exigua (Hiibner) (Jefferson et al. 1970), and Pseudaletia uni-
puncta (Haworth) (Lavoie & McNeil 1987). Typically, scales occur along with sensilla on
the surface of the noctuid antenna. Van der Pers et al. (1980), do not believe that scales
protect the sensilla from mechanical damage, but rather suggest that their disposition
contributes to the insect's ability to detect the direction of the stimulus. Wall (1978) ar-
gued that scales may be a mechanism to trap and concentrate odorous molecules.
The B6hm hairs of C. consueta are morphologically similar to those present in the
scape and the pedicel of the antenna of T ni, H. zea, S. ornithogalli, S. exigua (Jefferson
et al. 1970), and a pyralid (Cornford et al. 1973). Schneider (1964) suggested they have
a mechano-sensitive function. Similarly, Cuperus (1983) argues that these hairs in an
yponomeutid may have a mechano-receptor function at the scape-pedicel junction.
There is sexual dimorphism in C. consueta antennae. The antenna of the male has
a large number of long trichoid sensilla which are absent in the female. The presence
of these sensilla has also been reported in other noctuids: H. zea (Callahan 1969),
T ni, H. zea, S. ornithogalli and S. exigua (Jefferson et al. 1970). It has been demon-
strated in several moths that the long trichoid sensilla on the antenna of the male are
receptors for the sex pheromone of the female (Boekh et al. 1965, Schneider & Stein-
brecht 1968, Van der Pers & Den Otter 1978, Kaissling 1979, Zacharuk 1985).
Chaetica sensilla of C. consueta are similar in structure to those reported for other
noctuids by Callahan (1969), Jefferson et al. (1970), and Liu & Liu (1984). They were
suggested to be contact chemoreceptors in T ni, S. ornithogalli and S. frugiperda (J. E.
Smith) (Jefferson et al. 1970) and a tortricid (Albert & Seabrook 1973), but to have a
mechanoreceptive function in a mosquito (Davis & Socolove 1975) and in
























TABLE 2. DIMENSION OF THE SENSILLA ON THE ANTENNA OF COPITARSIA CONSUETA (WALKER).

Dimension of the sensilla X + sem (pm)

Male Female

Type of sensillum Length Width Length Width

Lateral 218.4 + 5.76 4.40 + 0.09 -
chemoreceptive trichoid (160.7-261.2) (3.27-4.91)
Ventral 74.2 4.28 3.23 0.1 34.81 1.34 1.76 0.04
chemoreceptive trichoid (45-100) 2.38 + 3.80 (26.25-42.85) (1.7-2.17)
Long (4) 108.27 + 12.47 4.96 + 0.40 86.89 + 6.79 4.62 + 0.32
mechanoreceptive chaetica (63.79-175.86) (3.44-6.89) (44.82-127.58) (3.44-6.89)
Short (2) 65.17 + 3.18 3.44 + 0.35 67.10 + 4.61 3.55 + 0.1
mechanoreceptive chaetica (53.44-68.96) (3.10-3.79) (41.37-82.75) (3.44-5.17)
Styloconic 2.58 + 0.04 2.20 + 0.04
(2.41-2.75) (2.06-2.41)
Coeloconic 10.44 0.45* 11.13 0.55* -
(8.62-13.79) (8.62-13.79)

n = 15 sensilla. *refers to diameter (range in parentheses).

















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December, 1999


TABLE 3. AVERAGE NUMBER OF SENSILLA ESTIMATED ON THE ANTENNA OF COPITARSIA
CONSUETA (WALKER).

Number of sensilla X + sem

Type of sensillum Male Female

Lateral 2814 + 144.6*
chemoreceptive trichoid (2481-3335)
Ventral 3477 36.4* 3298 186.64*
chemoreceptive trichoid (3266-3680) (3168-3562)
Long (4) 302.4 + 1.82a 309.2 + 2.31a
mechanoreceptive chaetica (284-320) (288-332)
Short (2) 151.13 + 0.93a 154.53 + 1.13a
mechanoreceptive chaetica (142-160) (144-162)
Styloconic 72.6 + 0.45a 74.3 + 0.580
(68-77) (69-79)
Coeloconic 422.9 + 17.18* 419.9 + 2.97*
(326-545) (405-463)

n = 10 antennae, an = 30 antennae (range in parentheses).



yponomeutids (Van der Pers & Den Otter 1978). Type I has a constant length in all an-
tennal segments, type II is smaller in the proximal segments, but increases in length
towards the distal segments of the flagellum, equaling the previous ones in size in
both sexes. These types also occur in H. zea (Callahan 1969), P. unipuncta (Lavoie &
McNeil 1987), and a pyralid (Cornford et al. 1973). A similar, but distinct, form occurs
in males of a tortricid (Wall 1978).
The presence of styloconic sensilla with double or triple apical structure is common
in noctuids: T ni, H. zea, P. ornithogalli and S. exigua (Jefferson et al. 1970), P. uni-
puncta (Lavoie & McNeil 1987) and Mamestra configurata Walker (Liu & Liu 1984).
In another tortricid, (Adoxophyes orana F. von R.), similar structures have been re-
ported as cuspiform organs (Den Otter et al. 1978).
Styloconic sensilla of C. consueta lack pores. However, pores occur on the stalk
near the reticulated base in P. unipuncta (Lavoie & McNeil 1987), at the apex in a
pyralid (Faucheux 1991), and at the side of the apex in a tortricid (Wall 1978). These
pored sensilla are thought to be chemoreceptors (Albert & Seabrook 1973), or, as in
H. zea, contact chemoreceptors (Callahan 1969). However, in yponomeutids, they may
have some other sensory function because they are located under scales where contact
chemoreception is not likely (Van der Pers et al. 1980).
Coeloconic sensilla, mostly present on each segment of males and females of C. con-
sueta from the medial to the distal part have also been found in other noctuids,
S. unipuncta (Lavoie & McNeil 1987) and M. configurata (Liu & Liu 1984), and a tor-
tricid (Albert & Seabrook 1973), and a pyralid (Cornford et al. 1973). Three to four sen-
silla occur per segment of males and females in C. consueta and in pyralids (Cornford
et al. 1973, Faucheux 1991). There was no size variation in these sensilla on the an-
tennae of either sex of C. consueta. This was not the case in an a tortricid examined by
Wall (1978). Such sensilla have been considered to be temperature receptors in a mos-
quito (Davis & Sokolove 1975) and a cockroach. In the latter insect, they are also sen-
















Castrejon et al.: Sense Organs of Copitarsia consueta


Fig. 5. Central portion of antennal flagellum of a female. Sensillum chaeticum type
I = Ch I and type II = Ch II; Sty = sensillum styloconicum. Bar = 100 Pm. Fig. 6. Sen-
sillum styloconicum (Sty). Cn = conical extremity with triple apical structure; Rb = re-
ticulated base; Ss = smooth stalk. Bar = 10 pm. Fig. 7. Sensillum coeloconicum (Co).
Sp = spike, Te = teeth. Bar = 10 pm. Fig. 8. Basiconic sensilla. Type I = BI, Type II =
BII. Bar = 10 pm.

















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December, 1999


sitive to humidity (Altner et al. 1977). However, their ultrastructure suggests they are
olfactory receptors, possibly sensitive to volatile odors of plants (Van der Pers 1981).
Basiconic sensilla are shorter than the ventral chemoreceptive trichoids, the apex
is rounded and they are located among the trichoids. Similar structures have been re-
ported for a tortricid (George & Nagy 1984) and an yponomeutid (Cuperus 1983). Cu-
perus (1983) and Faucheux (1991) observed pores in a basiconic sensilla. The presence
of this pores suggests an olfactory function, perhaps the reception of volatile odors of
plants (Van der Pers 1981).
Squamiform sensilla are similar to those described in an yponomeutid by Cuperus
(1983) and in a pyralid by Faucheux (1991). In the yponomeutid they were positioned
on the scape, the pedicel, and the first 5 segments of the flagellum, but in C. consueta
they occur as far as the middle of the flagellum. Lavoie & McNeil (1987) observed such
sensilla laterally on the ventral surface of each antennal segment in P. unipuncta, but
we found them in a transverse line on the entire ventral surface of the antennal seg-
ments of C. consueta.


ACKNOWLEDGMENTS

We thank Dr. J. H. Frank (Entomology and Nematology Department, University of
Florida) for guidance and corrections to a manuscript draft. We also thank CONACYT
and I.P.N.- for the grants DEPI 980052 and COFAA-I.P.N.

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VAN DER PERS, J. N. C., P. L. CUPERUS, AND C. J. DEN OTTER. 1980. Distribution of
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6. Pergamon Press, Oxford.
















Florida Entomologist 82(4)


December, 1999


EVALUATION OF ERETMOCERUS EREMICUS AND ENCARSIA
FORMOSA (HYMENOPTERA: APHELINIDAE) BELTSVILLE
STRAIN IN COMMERCIAL GREENHOUSES FOR BIOLOGICAL
CONTROL OF BEMISIAARGENTIFOLII (HOMOPTERA:
ALEYRODIDAE) ON COLORED POINSETTIA PLANTS

MARK S. HODDLE'2 AND ROY VAN DRIESCHE'
'Department of Entomology, University of Massachusetts, Amherst, MA 01003.

2Current address: Department of Entomology, University of California,
Riverside, CA 92521.

ABSTRACT

The effectiveness of average weekly inundative releases of female Eretmocerus er-
emicus (evaluated in 2 greenhouses) and Encarsia formosa Beltsville strain (evalu-
ated in 2 greenhouses) per plant for control ofBemisia argentifolii Bellow and Perring
was determined on colored poinsettia plants grown under commercial conditions. Par-
asitoid efficacy was determined by making weekly population counts ofB. argentifolii
lifestages (excluding eggs) on plants exposed to parasitoids in biological control green-
houses and comparing final per leaf densities ofB. argentifolii nymphs to those plants
in insecticide treated greenhouses. At the 2 sites where E. eremicus was used, final
nymphal densities ranged from 2-4 per leaf when a sales inspection protocol was em-
ployed at time of harvest. On insecticide-treated plants, nymphs ranged 0.02-0.18 per
leaf but final whitefly densities in biological control greenhouses and insecticide
greenhouses were commercially acceptable. Colored plants at one site where E. ere-
micus was used were harvested and sold without any insecticide use. At the second E.
eremicus site, two sulfotepp applications were made at week 11 of the 16 week trial
and colored plants were harvested without further use of insecticides. In comparison
to insecticides, the cost ofE. eremicus in 1995 ($2.70 per plant) was 30 times higher
than using imidacloprid ($0.09 per plant) for B. argentifolii control. At the 2 sites
where E. formosa Beltsville strain was released, trials were terminated early and in-
secticides were applied when B. argentifolii densities reached 4-6 live nymphs and pu-
pae per leaf. Low emergence rates of E. formosa Beltsville strain may have been a
major factor lowering the efficacy of this parasitoid in commercial greenhouses.

RESUME

En invernaderos comerciales se liberaron semanalmente hembras de Eretmocerus
eremicus (dos invernaderos) y de Encarsa formosa raza Beltsville (otros dos inverna-
deros) para el control de Bemisia argentifolii Bellow y Perring en plants de noche-
buena colorida. La efectividad de los parasitoides se evalu6 realizando conteos
semanales de los estadios de B. argentifolii excepto huevecillos) en plants expuestas
a los parasitoides en invernaderos de control biol6gico y en invernaderos tratados con
insecticides. La densidad final de ninfas de B. argentifolii por hoja fue comparada en-
tre plants provenientes de invernaderos de control biol6gico y de aquellos tratados
con insecticide. Cuando se emple6 E. eremicus, las densidades finales de ninfas varia-
ron de 2-4 por hoja en el moment de realizar una inspecci6n de protocolo para venta
de las plants. En plants tratadas con insecticide, la densidad de ninfas vari6 de
0.02-0.18 por hoja, pero la densidad final de mosquitas en plants tratadas con control
biol6gico o quimico fue comercialmente acceptable. En uno de los invernaderos donde
se utilize E. emericus, las plants fueron cosechadas y vendidas sin haberse empleado
insecticides. En el otro invernadero donde fue empleado E. emericus, las plants reci-
bieron dos aplicaciones de sulfotepp (semanas 11 y 16 del ensayo), despues de lo cual

















Hoddle & Van Driesche Control of Bemisia argentifolii 557

fueron cosechadas sin mas uso de insecticides. En 1995, el costo de controlar B. argen-
tifolii con E. emericus fue 30 veces mayor al de usar el insecticide imidacloprid ($2.70
vs. $0.09 por planta. En los dos invernaderos donde se us6 E. formosa raza Beltsville,
los ensayos fueron suspendidos temprano y se aplic6 insecticide cuando las densida-
des de B. argentifolii alcanzaron 4-6 ninfas vivas y pupas por hoja. Las tasas de emer-
gencia de E. formosa raza Beltsville fueron bajas, lo cual pudo haber sido un factor
important en la baja efectividad de este parasitoide para controlar B. argentifolii en
invernaderos comerciales.





Inundative biological control of whitefly pests infesting greenhouse-grown orna-
mentals is seldom practiced by commercial producers and chemically based pest con-
trol strategies prevail. Several reasons for lack of adoption of biological control by
growers of greenhouse ornamentals have been identified and include: (1) the high cost
of purchasing natural enemies for mass release makes pesticides more attractive fi-
nancially; (2) inconsistent natural enemy quality, quantity, and availability from com-
mercial suppliers can adversely affect programs making growers wary of biological
control; (3) a paucity of rigorous research documenting efficacy and economic cost of
biological control makes justification of biological control implementation difficult; (4)
lack of crop and pest specific management guidelines with natural enemies for grow-
ers to follow means there is no established infrastructure similar to that available for
pesticides with which growers are familiar (Cranshaw et al. 1996, O'Neil et al. 1998,
Parrella & Jones 1987, Parrella 1990, Parrella et al. 1992, Hoddle et al. 1997, Wearing
1988). In this article we address issues which concern natural enemy efficacy and
quality, and the cost effectiveness of biological control for silverleaf whitefly, Bemisia
argentifolii Bellows & Perring (Homoptera: Aleyrodidae), on colored poinsettias (Eu-
phorbia pulcherrima Willd. ex Koltz.) grown under commercial conditions.
Eretmocerus eremicus Rose and Zolnerowich (Hymenoptera: Aphelinidae) has
been identified as an effective natural enemy ofB. argentifolii (Hoddle et al. 1998a).
Weekly releases of three female parasitoids per plant per week obviated the need for
pesticides on non-colored poinsettias commercially grown for cuttings, and use of
E. eremicus is recommended for control ofB. argentifolii on poinsettia stock plants in
summer (Hoddle & Van Driesche 1999). However, the ability ofE. eremicus to control
B. argentifolii on colored poinsettia plants grown in the fall was uncertain at the time
of this trial. Weekly releases ofE. eremicus in small experimental greenhouses where
the release rate was varied over time failed to control B. argentifolii on colored poin-
settia plants grown in the fall suggesting that this parasitoid and release strategy
may be unsuitable for use at this time of year (Hoddle et al. 1999). The efficacy of con-
stant weekly releases of E. eremicus for B. argentifolii control on colored poinsettia
plants during normal fall production periods had not been previously determined in
commercial greenhouses at the time work presented here was done.
Encarsia formosa Gahan Beltsville strain (Hymenoptera: Aphelinidae) is a Bemi-
sia-adapted strain of E. formosa (Heinz & Parrella 1994). Use of this parasitoid in
small experimental greenhouses at a rate of three females per plant per week pro-
duced final densities ofB. argentifolii on colored poinsettias that were indistinguish-
able from those on plants produced commercially with pesticides for sale at Christmas
(Hoddle et al. 1997). However, in commercial greenhouses E. formosa Beltsville strain
failed to control B. argentifolii on poinsettias grown for cuttings during summer
whereas under similar conditions E. eremicus provided acceptable control ofB. argen-
tifolii (Hoddle & Van Driesche 1999).

















Florida Entomologist 82(4)


December, 1999


These results suggest that E. eremicus is the more effective natural enemy for B.
argentifolii control on stock plants grown in summer and that E. formosa Beltsville
strain might be more effective on colored poinsettias grown in the fall. The ability of
E. formosa Beltsville strain to control B. argentifolii on commercially produced col-
ored poinsettias, however, has not been determined. Here we present results that
compare the efficacy of E. formosa Beltsville strain to that of E. eremicus against B.
argentifolii under commercial growing conditions on poinsettias grown in the fall for
sale at Christmas.

MATERIALS AND METHODS

Experimental Greenhouses

This experiment was conducted with four commercial growers in Massachusetts,
USA, using either E. eremicus (two growers) or E. formosa Beltsville strain (two grow-
ers) for B. argentifolii control in greenhouses on colored poinsettia plants grown for
the Christmas market. Evaluation trials were run over the period 4 August to 7 De-
cember, 1995.
Site one was a 260-m2 glass greenhouse containing 3,200 plants. Cultivars grown
were "Red Sails", red "Lilo", and white and marble "Angelika". Site two was a 156-m2
glass greenhouse containing 2,300 plants. Cultivars grown were white and marble
"Annette Hegg", red "Lilo", red "Celebrate 2", and "Pink Peppermint". Sites one and
two received weekly releases ofE. eremicus and plants were reduced in number dur-
ing the trial to satisfy spacing and sales requirements. Site three was a 168-m2 plastic
greenhouse with 1,800 plants. A single cultivar, white "Glory V-14", was grown at this
site. Site four was a 307-m2 glass greenhouse, stocked with 2,881 plants. Cultivars
grown were "Celebrate 2", marble "Angelika" and pink "Gutbier V-14". Sites three and
four received weekly releases of E. formosa Beltsville strain.

Estimating Initial Whitefly Infestation Levels
and Augmentation of Whitefly Numbers

The colored crops at sites 1 and 2 were started from rooted cuttings produced by
each grower in the spring, using cuttings that had been produced using E. eremicus
as the sole control strategy for B. argentifolii (Hoddle & Van Driesche 1999). Cuttings
at sites 3 and 4 were produced in-house by the growers and B. argentifolii had been
controlled chemically on stock plants with foliar insecticides before cuttings were har-
vested and held for three weeks in misting units for rooting. At the time of potting at
each site, 70-90 randomly selected cuttings were numbered. Each leaf on the num-
bered cuttings was examined and total numbers of live B. argentifolii nymphs and pu-
pae (one sampling category), and adults per plant were recorded. The average number
of nymphs and pupae, and adult whiteflies per plant was calculated for each site and
compared using a one-way ANOVA in SAS (SAS 1989) and Tukey's Studentized
Range Test (P = 0.05) was used for means separation. At sites 2, 3, and 4 control and
parasitoid release cages were stocked with poinsettia plants infested at the same
nymphal and pupal density as that occurring in their respective biological control
greenhouses (see below for more details on the use of cages). At site 1, all plants ex-
amined were free ofB. argentifolii and augmentative releases of adult whiteflies were
made to establish a pest population in the biological control greenhouse. The control
and parasitoid release cages were also artificially inoculated with adult whiteflies at
the same rate as the biological control greenhouse.

















Hoddle & Van Driesche Control of Bemisia argentifolii 559

Whitefly augmentation. Because no whiteflies were seen on cuttings at site 1, the
whitefly population there was augmented by introducing adult male and female pairs
of B. argentifolii from our laboratory colony. Our intention was to introduce adult
whiteflies to produce similar average per plant densities as that observed across all
greenhouses at the time of planting. To do this we released 332 adult whiteflies (166
mating pairs) into the biological control greenhouse which held 3,200 plants at time
of release (week 2 of the trial). This produced an average of 0.1 adult whiteflies per
plant. The control cage and parasitoid release cage at site 1 (all cages contained 10
plants) were stocked with one male-female pair of adult B. argentifolii at the same
time.


Experimental Treatments & Weekly Population Counts for B. argentifolii

Three treatments were established in each of the four biological control green-
houses: uncaged plants (Treatment 1), cages with whiteflies only (Treatment 2), and
cages with parasitoids and whiteflies (Treatment 3). Treatment 2 was the control, and
Treatment 3 acted as a check for cage effects for whitefly development in the presence
of parasitoids.
To estimate whitefly population densities on uncaged plants, three leaves (one
from the bottom, one from the middle, and one from the top) of 90 plants in all exper-
imental greenhouses were inspected weekly for the presence of B. argentifolii. The
numbers of nymphs and pupae, adults, and whitefly exuviae from which either adult
whiteflies or parasitoids had emerged were recorded along with numbers of visibly
parasitized whitefly nymphs. Weekly population counts were made at each site until
either the grower harvested colored plants or applied insecticides because whitefly
numbers had reached unacceptable densities. Final densities of live nymphs and pu-
pae per leaf for Treatment 1 in each greenhouse were compared using a nested
ANOVA in SAS (SAS 1989) and Tukey's Studentized Range Test (P = 0.05) was used
for means separation.


Establishing & Monitoring B. argentifolii Population Growth in Cages

Treatments 2 and 3 were established in single cages in each of the four biological
control greenhouses. Cages measured 153 cm (length) x 92 cm (width) x 117 cm
(height), were constructed of pvc piping, and were enclosed on all sides with polyester
mesh screening with a 95 pm opening size. Access to plants within cages was via two
sleeves in the front of the cage and whiteflies were counted through a clear acetate
panel located between the sleeves. Each cage was stocked with 10 potted poinsettia
plants that were chosen from those examined to estimate the initial infestation level
at planting. We stocked cages with selected plants to achieve similar average densi-
ties of live nymphs and pupae per plant as those in the corresponding biological con-
trol greenhouses.
For Treatments 2 and 3, whitefly population density estimates were made weekly
on eight randomly selected plants within cages. In Treatment 3, parasitoids were re-
leased into cages at a rate of three female parasitoids per plant per week. Based on an
expected 50:50 sex ratio and an emergence rate of 60%, 100 Trialeurodes uaporari-
orum (Westwood) (Homoptera: Aleyrodidae) nymphs parasitized by E. eremicus were
placed weekly in cages at sites 1 and 2 in a single release cup. In the E. formosa Belts-
ville strain release cages at sites 3 and 4, 50 parasitized B. argentifolii nymphs were
placed in cages weekly. We assumed a 60% emergence rate and an all female popula-
tion for this parasitoid.

















Florida Entomologist 82(4)


December, 1999


Monitoring of Insecticide-Treated Greenhouses, end of Trial Whitefly Densities,
& Cost Analysis

To measure the performance of parasitoids compared to conventional whitefly con-
trol practices, two greenhouses treated with insecticides, one at site one and one at
site three, were monitored weekly. Live B. argentifolii nymphs and pupae were
counted on each of three randomly selected leaves (one leaf from the bottom, middle,
and top of the plant) on 90 randomly selected plants. Mean numbers of live whitefly
nymphs and pupae per leaf were compared to those observed in the biological control
greenhouses and parasitoid release cages.
The average number of live whiteflies per leaf was determined using a sampling
protocol used from previous studies (Hoddle et al., 1998a, 1999). Fifteen plants were
randomly selected from each experimental greenhouse and the number of live white-
fly nymphs and pupae were recorded for each of six leaves (two leaves were chosen at
random from the bottom, middle, and top of the plant.)
The cost of biological control versus the cost of insecticides was determined at site
1 by analyzing insecticide application records for the insecticide-treated greenhouse,
and the cost of using E. eremicus in the biological control greenhouse at the same site.
The cost of whitefly control using imidacloprid (a systemic chloronicotinyl compound
[Cahill et al. 1996]) was based on 1995 catalogue prices for Marathon (a granular in-
secticide of 1% imidacloprid, [Olympic Horticultural Products, Mainland, PA]). The
cost of using E. eremicus was based on the 1995 retail figure of $22 for 1000 parasit-
ized T vaporariorum nymphs. Encarsia formosa Beltsville strain was sold to us for $9
per 1000 parasitized B. argentifolii nymphs.

Estimating Weekly Parasitoid Release Rates

Parasitoid releases in the biological control greenhouses and parasitoid cages be-
gan immediately after greenhouses were filled with poinsettias. The targeted weekly
release rate for both parasitoid species was three females per plant per week. Eret-
mocerus eremicus is a bi-parental species (sex ratio is 1:1) and was supplied by Bene-
ficial Insectaries, Oak Run, California USA, as loose parasitized T vaporariorum
nymphs which had been reared on tobacco. Encarsia formosa Beltsville strain is a uni-
parental parasitoid, which was reared on B. argentifolii on collard greens and supplied
by American Insectaries, Escondido, California USA, 25 loose parasitized nymphs.
Parasitized nymphs were distributed throughout greenhouses and cages by plac-
ing them in plastic release cups (height 3 cm; diameter, 4 cm). Release cups were at-
tached to stakes that were pushed into the potting media until cups were positioned
below the crop canopy. To estimate the number of parasitoids released per plant per
week, we measured the number of nymphs per unit weight of material sent by the
supplier, the weight of the shipment, and the percentage of nymphs from which par-
asitoids successfully emerged under greenhouse conditions. Percentage emergence
was determined by returning release cups every two weeks to the laboratory and re-
cording the number of nymphs from which parasitoids did and did not emerge. We as-
sumed a 1:1 sex ratio for E. eremicus in our calculations.


RESULTS

Initial Whitefly Infestation Levels on Cuttings at Potting

There was a significant difference across sites in the mean number (+ SE) of live
nymphs and pupae on cuttings at the time of planting (F = 44.5, df= 3, p = 0.0001). At

















Hoddle & Van Driesche Control of Bemisia argentifolii 561

sites 1, 2, (both E. eremicus) 3, and 4 (both E. formosa Beltsville strain), the average
number of live nymphs and pupae per plant was 0.00 + 0.00 (n = 90 cuttings) (because
no immature whiteflies were found at site 1 it was not included in the ANOVA), 8.19
+ 0.78 (n = 70) [a], 5.86 + 0.84 (n = 90) [b], and 1.41 + 0.18 (n = 90) [c], respectively.
Means followed by the same letters are not significantly different from each other.
Both the E. eremicus and E. formosa Beltsville strain treatments had one relatively
high and one relatively low initial density of whiteflies.
There was also a significant difference across site in the mean number (- SE) of
adult whiteflies per plant at time of potting (F = 8.32, df = 2, p < 0.00001). At sites 1,
2, 3, and 4, the average number of live adults per plant was 0.00 + 0.00 (because no
adult whiteflies were found at site 1 it was not included in the ANOVA), 0.06 + 0.02
[a], 0.4 + 0.09 [b], 0.1 + 0.05 [a], respectively. Means followed by the same letters are
not significantly different from each other. The average number of adult whiteflies per
plant when averaged across all biological control greenhouses (n = 4) was 0.16 + 0.03.

Actual Parasitoid Release Rates

Emergence rates of adult parasitoids in the two E. eremicus greenhouses averaged
53.8% + 4.8% and 55.6% + 3.9% for sites 1 and 2 across the entire trial periods, respec-
tively (Table 1). In the two E. formosa Beltsville greenhouses, weekly percentage emer-
gence of adult parasitoids averaged 33.0% + 3.8% and 38.3% + 5.6% for sites 3 and 4,
respectively (Table 1). The average number of female parasitoids released per plant
per week at sites 1 and 2 was 2.9 + 0.2 and 3.7 + 0.31 respectively, for the two E. ere-
micus greenhouses (Table 1). The average number of female parasitoids released at
sites 3 and 4 was 1.9 + 0.25 and 2.4 + 0.37 per plant per week, respectively (Table 1).
This average weekly release rate for E. formosa Beltsville strain were lower than the
intended release rate of 3 females per plant per week because of poor emergence of par-
asitoids following deployment of parasitized B. argentifolii nymphs in greenhouses.

Population Density Trends for B. argentifolii

Population growth of B. argentifolii in cages in the absence of E. eremicus (Treat-
ment 2) was substantially higher than that observed for populations receiving para-
sitoid releases (Treatment 3) (Fig. 1). In control cages at the end of the trials, numbers
of live nymphs and pupae exceeded 29 and 117 per leaf at sites 1 and 2, respectively.
At the end of the trials in cages treated with E. eremicus, populations of live B. argen-
tifolii nymphs and pupae per leaf reached 8 and 2 at sites 1 and 2, respectively,
(Fig. 1). Upon grower request, cages at sites 3 and 4 where E. formosa Beltsville strain
was released were removed and trials were terminated in weeks 6 and 4, respectively
when insecticides were applied for whitefly control. No useful data was obtained from
cages studies at sites 3 and 4 because trials were terminated before B. argentifolii
population trends became evident.
Colored poinsettia plants were harvested at site 1 without the use of any insecti-
cides. Two insecticide applications were required at site 2 to reduce numbers of adult
whiteflies on plants (Fig. 2). The biological control greenhouse was treated with two
sulfotepp fumigations (Plantfume smoke generator, ai 15% sulfotepp [Plant Products
Corporation, Vero Beach FL]) three days apart during week 11 of the trial. Parasitoid
releases continued after fumigation and plants were harvested at week 16 without
further insecticide intervention. In greenhouses receiving releases of E. eremicus
(sites 1 and 2), densities of live nymphs and pupae were less than two per leaf when
trials ended. This final density of live nymphs and pupae was acceptable to commer-
cial growers producing colored poinsettias for sale at Christmas (Fig. 2).


















Florida Entomologist 82(4) December, 1999


TABLE 1. TOTAL NUMBER OF PLANTS, TOTAL NUMBER OF PARASITIZED NYMPHS PLACED
IN GREENHOUSES, PERCENTAGE PARASITOID EMERGENCE, AND NUMBER OF FE-
MALE PARASITOIDS RELEASED PER PLANT IN BIOLOGICAL CONTROL GREEN-
HOUSES TREATED WEEKLY WITH ERETMOCERUS EREMICUS AND ENCARSIA
FORMOSA BELTSVILLE STRAIN.

No.
No. Parasitoid females
Week parasitized Emergence released/
Wasp Site no. Plant no. nymphs (%) plant

E. eremicus 1 1 3.200 no releases


mean (t SE)


E. eremicus 2


3,200
2,550
2,550
1,969
1,219
1,219
1,500
800
1,081
500
500
500
500



2,300
2,300
2,300
1,250
900
621
621
621
621
621
621
621
621
621
621
621



1,800
1,800


mean (- SE)


E. formosa 3


29,023
25,552
25,238
19,722
12,360
12,213
6,572
8,015
10,816
5,009
8,339
8,349
8,343


53.8 + 4.8 2.9 + 0.2


23,023
23,045
12,518
9,016
6,219
6,212
6,217
10,360
10,370
10,370
10,369
10,368
10,361
10,360
10,360


55.6 3.6 3.7 0.31


9,000 31.3
9,000 45.3

















Hoddle & Van Driesche Control of Bemisia argentifolii 563

TABLE 1. (CONTINUED) TOTAL NUMBER OF PLANTS, TOTAL NUMBER OF PARASITIZED
NYMPHS PLACED IN GREENHOUSES, PERCENTAGE PARASITOID EMERGENCE,
AND NUMBER OF FEMALE PARASITOIDS RELEASED PER PLANT IN BIOLOGICAL
CONTROL GREENHOUSES TREATED WEEKLY WITH ERETMOCERUS EREMICUS
AND ENCARSIA FORMOSA BELTSVILLE STRAIN.

No.
No. Parasitoid females
Week parasitized Emergence released/
Wasp Site no. Plant no. nymphs (%) plant

3 1,800 9,000 24.6 1.23
4 1,800 18,007 26.6 2.66
5 1,800 8,992 37.3 1.86
6 1,800 15,875 -
mean (_ SE) 33.0 + 3.8 1.9 + 0.25

E. formosa 4 1 2,881 20,000 23.3 1.60
2 2,881 16,000 39.3 2.17
3 2,881 16,281 40.0 2.26
4 1,508 8,680 50.6 3.38
mean (_ SE) 38.3 + 5.6 2.4 + 0.37



Parasitism Levels

Parasitism by E. eremicus in the biological control greenhouse was first recorded
at week 2 at site 2, and steadily increased to reach a maximum of 43% before declining
to 15% at the end of the trial (Fig. 3). In contrast, parasitism by E. eremicus at site 1
was not detected until week 6. Peak parasitism by E. eremicus at site 1 reached 30%
at week 8 and then declined to 4-7% for the last four weeks of the trial (Fig. 3). Para-
sitism did not exceed 5% in the biological control houses at the two sites in which
E. formosa Beltsville strain was released (Fig. 3).


Insecticide-Treated Greenhouses

Insecticide-treated greenhouses at sites 1 and 3 received one application each of
imidacloprid (Marathon) immediately after greenhouses were filled. This insecticide
can give up to 12 weeks protection with a single application (Lopes 1994).


Whitefly Densities at Harvest

The protocol designed to evaluate the mean number of live nymphs and pupae per
leaf at time of harvest on 15 randomly selected plants detected significant differences
between both sites 1 and 2 treated with E. eremicus and to numbers recorded on
plants in retail outlets (F = 37.94, df = 2, p = 0.0001) (Table 2). Weekly releases of
E. formosa Beltsville strain failed to reduce B. argentifolii to non-damaging densities
and trials at sites 3 and 4 were terminated early and insecticides were applied to the
crop prior to the harvesting of colored plants. Consequently, similar comparisons of
whitefly numbers in the biological control greenhouses at sites 3 and 4 with insecti-
cide treated plants were not made.

















Florida Entomologist 82(4)


December, 1999


150 -
140
2 130
S120-
110 -
S100
90
S80
E 70
z 60-
50
6 40 /
Z 30-/
20
10

1 2 3 4 5 6 7 8 9 10 11 12 13 14
Week Number of Trial

,---Control Cage (Site 1) ---Control Cage (Site 2)
-o- Eretmocerus eremicus Release Cage (Site 1) --- Eretmocerus eremicus Release Cage (Site 2)

Fig. 1. Mean number of live Bemisia argentifolii nymphs and pupae (+ SE) per leaf
on poinsettia plants in the control and parasitoid release cages in the biological con-
trol greenhouses treated with E. eremicus.

Cost Analysis

At site 1, the total cost of controlling B. argentifolii with an average weekly release
rate of 2.9 female E. eremicus per plant for 14 weeks was 30 times more expensive
than the use of imidacloprid for whitefly control (Table 3). Cost analysis for use of
E. formosa Beltsville strain at site 3 was not calculated as this trial was terminated
early following grower intervention with foliar insecticide applications.

DISCUSSION

Releases ofE. eremicus at rates of 2.9-3.7 females per plant per week successfully
suppressed B. argentifolii to non-damaging levels on colored poinsettias. The sales in-
spection protocol detected 2-4 live B. argentifolii nymphs and pupae per leaf and
plants were marketable with this level of whitefly infestation at harvest. Mean den-
sities of live B. argentifolii nymphs and pupae per leaf on the 90 randomly selected
plants at sites 1 and 2 were both less than two (compared to 2-4 live nymphs and pu-
pae from the sales inspection protocol) when trials were ended and plants were har-
vested. This larger sample size may have resulted in a more accurate assessment of
final per leaf densities ofB. argentifolii at time of harvest indicating that final densi-
ties of live B. argentifolii nymphs and pupae per leaf being less than two are commer-
cially acceptable.
In one of the two E. eremicus greenhouses (site 1) the crop was harvested without
any insecticide applications even though B. argentifolii were I. 11... .. l introduced
to produce an initial infestation of 0.1 adult whiteflies per plant, a density similar to
that seen in the other biological control greenhouses. At site 1, initial inspection of


















Hoddle & Van Driesche Control of Bemisia argentifolii 565

7


0) 6-







4-
u (
5A
z








0 ,-,-,l, --,
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Week Number of Trial

-0-- Eretmocerus eremicus (Site 1) --Eretmocerus eremicus (Site 2)
-o-Encarsia fom~sa Beltsville strain (Site 3) --Encarsia formosa Beltsville strain (Site 4)

Fig. 2. The mean number of live Bemisia argentifolii nymphs and pupae (_ SE) per
leaf on uncaged poinsettia plants in the biological control greenhouses treated with
Eretmocerus eremicus (sites 1 and 2) or Encarsia formosa Beltsville strain (sites 3 and
4). Trial duration times at sites 3 and 4 were reduced because growers intervened
with chemical treatments to suppress B. argentifolii population growth. Arrows indi-
cate times of insecticide applications at site 2.


cuttings failed to detect whitefly nymphs prior to parasitoid releases beginning and
whitefly nymphs were not I.. I... :i,.. introduced to produce initial nymph densities
similar to those seen in the other biological control greenhouses. Because initial
whitefly densities at site one were low, whitefly numbers remained consistently lower
throughout the duration of the trial and the test ofE. eremicus for B. argentifolii con-
trol was not as rigorous as site 2. At the second E. eremicus release site (site 2) initial
whitefly densities were higher than site 1, and biological control was successfully
combined with two fumigatory sulfotepp applications to produce commercially accept-
able colored plants.
Data collected at harvest indicates that growers and consumers are tolerant of
light whitefly infestations on colored poinsettias and biologically based control pro-
grams do not have to achieve zero whitefly densities for plants to be marketable. Tri-
als subsequent to this one have demonstrated that E. eremicus can also successfully
control another common whitefly pest of poinsettia, T vaporariorum, on colored
plants and that growers are able to successfully manage their own biological control
program using this parasitoid under commercial growing conditions (Van Driesche et
al. 1999a).
A major obstacle to the use ofE. eremicus for biological control ofB. argentifolii on
greenhouse grown poinsettias is the high cost of this parasitoid in comparison to in-
secticides for control of this pest. The use of E. eremicus for control B. argentifolii on

















Florida Entomologist 82(4)


December, 1999


50-

45

40-

E 35
4 30





10





1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Week Number of Trial

-C- Eretmocerus eremicus (Site 1) -W- Eretmocerus eremicus (Site 2)
--Enarsia formosa Beltsviffe strain (Site 3) -- Encarsia formosa Beltsville strain (Site 4)

Fig. 3. Percentage parasitism of Bemisia argentifolii in biological control green-
houses treated with either Eretmocerus eremicus (sites 1 and 2) or Encarsia formosa
Beltsville strain (sites 3 and 4).


poinsettias grown for cuttings in 1995 was 44 times more expensive than using imi-
dacloprid (Hoddle & Van Driesche 1999). In this study with colored poinsettia plants,
E. eremicus was 30 times more expensive than the same insecticide in 1995. Since
1995 when this work was done the cost ofE. eremicus has decreased by 62% and this
parasitoid currently retails for $8.30 per 1000 parasitized T vaporariorum nymphs
(Hoddle & Van Driesche 1999). At the 1999 cost the use ofE. ermicus at site 1 in this
trial would have been $1.02 per single stem plant, or just 11 times more expensive
than imidacloprid.
The cost of using E. eremicus in a biologically based pest management program
can be reduced further by reducing the numbers of parasitoids released weekly. One
way of accomplishing a reduced weekly release rate is to combine E. eremicus with
compatible insect growth regulators (IGRs). We have identified IGRs that can be suc-
cessfully used with E. eremicus (Hoddle & Van Driesche unpublished). When E. ere-
micus is combined with two mid-season applications of Applaud 70 WP (ai 70%
buprofezin [Agrevo USA Company, Wilmington DE]) the weekly parasitoid release
rate can be reduced by 66%. Marketable colored poinsettias are produced under com-
mercial conditions using this parasitoid-IGR program at a cost of $0.38 per single
stem plant, a price more competitive with imidacloprid which can cost $0.09-$0.14 per
plant (Van Driesche et al. 1999b).
Encarsia formosa Beltsville strain failed to provide adequate control ofB. argenti-
folii at the two sites at which it was released. This result was due in part to low par-
asitoid emergence rates (33-38%) in experimental greenhouses. We did not determine
whether environmental factors in greenhouses (e.g., aspects of commercial poinsettia

















Hoddle & Van Driesche Control of Bemisia argentifolii 567

TABLE 2. INFESTATION STATISTICS FOR LIVE BEMISIA ARGENTIFOLII NYMPHS AND PUPAE
ON POINSETTIA LEAVES FROM EXPERIMENTAL GREENHOUSES AT TIME OF HAR-
VEST IN WHICH ERETMOCERUS EREMICUS HAD BEEN RELEASED, AND ON
LEAVES OF COLORED POINSETTIAS RECORDED FROM RETAIL OUTLETS AT THE
END OF THE 1995 GROWING SEASON.

No. plants % Plants No. leaves % Leaves Nymphs/
Treatment inspected infested examined infested Leaf SE

Site 1 15 87 45 58 3.8 0.9a
(E. eremicus)
Site 2
(E. eremicus) 15 93 45 56 1.9 + 0.8b
Five retail
outlets in
Amherst,
Massachusetts 75 11 225 4 0.08 + 0.03c
(chemical control)

Means followed by different letters are significantly different from each other at the 0.05 level of significance.


production that reduce efficacy of E. formosa Beltsville strain) or poor parasitoid qual-
ity were responsible for low emergence rates. Because of low rates of parasitoid emer-
gence, 89% of releases failed to reach the intended release rate of three parasitoids
per plant per week, a rate which has been shown to be efficacious in small greenhouse
trials (Hoddle et al. 1997). During the course of our work (1994-1995) with E. formosa
Beltsville strain two companies (one European and one American) attempted to com-
mercialize this parasitoid. Restructuring of the European insectary resulted in E. for-
mosa Beltsville strain being removed from its product line while persistent
production problems (i.e., disease and hyperparasitism by Encarsia pergandiella
Howard) hampered yield and promoted the ultimate loss of the only commercial
E. formosa Beltsville strain colony in the USA.
In addition to uncertainty of supply and post-receipt quality, inherent biological
attributes may have also prevented E. formosa Beltsville strain from being an effec-
tive natural enemy of B. argentifolii on poinsettias. Under time limited conditions in
commercial poinsettia-production greenhouses, E. formosa Beltsville strain is disad-
vantaged because it is slower in discovering B. argentifolii patches, finds fewer


TABLE 3. COMPARISON OF THE COSTS OF BEMISIA ARGENTIFOLII CONTROL AT SITE 1 IN
THE INSECTICIDE GREENHOUSE AND THE BIOLOGICAL CONTROL GREENHOUSE
TREATED WITH ERETMOCERUS EREMICUS.

Biological control
Insecticide greenhouse greenhouse

Total cost of imidacloprid $288.00 NA
Total cost of E. eremicus NA $3,950.12
Treatment cost per plant $ 0.09 $ 2.70
Cost m2 $ 1.11 $ 15.19

















Florida Entomologist 82(4)


December, 1999


patches, kills fewer whitefly nymphs upon patch discovery, and is observed less fre-
quently on patches when compared to similar studies with E. eremicus (Hoddle et al.
1998b). The inability of E. formosa reared on either B. argentifolii or T vaporariorum
(the standard insectary host for this parasitoid) to control B. argentifolii on poinset-
tias grown for cuttings (Parrella et al. 1991, Hoddle & Van Driesche 1999) or for color
(Hoddle & Van Driesche 1996) suggests this species cannot be recommended for B. ar-
gentifolii control on commercially grown poinsettias.
In contrast, the efficacy of E. eremicus for B. argentifolii control continues to be
supported by results of trials in poinsettia crops under various growing conditions.
Further work on developing programs which use E. eremicus in combination with se-
lective insecticides such as IGRs is needed before this parasitoid will be economically
competitive with currently employed control programs that rely exclusively on insec-
ticides.

ACKNOWLEDGMENTS

We thank Mr. P. Burnham, Mr. I. Seedholm, Mr. C. Olson, and Mr. W. Mendoza for
allowing us to conduct these experiments in their greenhouses. Susan Roy and Mark
Mazzola provided meticulous field and laboratory assistance. Our research was sup-
ported by funds from the Massachusetts Poinsettia IPM program, and USDA/
NRICGP Grant No. 9402481.

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CRANSHAW, W., D. C. SCLAR, AND D. COOPER. 1996. A review of 1994 pricing and mar-
keting by suppliers of organisms for biological control of arthropods in the
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HEINZ, K. M. AND M. P. PARRELLA. 1994. Poinsettia (Euphorbia pulcherrima Willd.
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rodidae). Biological Control 4: 305-318.
HODDLE, M. S. AND R. G. VAN DRIESCHE. 1996. Evaluation of Encarsia formosa (Hy-
menoptera: Aphelinidae) to control Bemisia argentfolii (Homoptera: Aley-
rodidae) on poinsettia (Euphorbia pulcherrima): a lifetable analysis. Florida
Entomologist 79: 1-12.
HODDLE, M. S., R. G. VAN DRIESCHE, AND J. P. SANDERSON. 1997. Biological control
of Bemisia argentifolii (Homoptera: Aleyrodidae) on poinsettia with inundative
releases of Encarsia formosa Beltsville strain (Hymenoptera: Aphelinidae): can
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Entomology 90: 910-924.
HODDLE, M. S., R. G. VAN DRIESCHE, J. P. SANDERSON, AND O. P. J. M. MINKENBERG.
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poinsettia with inundative releases of Eretmocerus eremicus (Hymenoptera:
Aphelinidae): do release rates affect parasitism? Bulletin of Entomological Re-
search 88: 47-58.
HODDLE, M. S., R. G. VAN DRIESCHE, J. S. ELKINTON, AND J. P. SANDERSON. 1998b.
Discovery and utilization of Bemisia argentifolii patches by Eretmocerus ere-
micus and Encarsia formosa (Beltsville strain) in greenhouses. Entomologia
Experimentalis et Applicata 87: 15-28.
HODDLE, M. S., J. P. SANDERSON, AND R. G. VAN DRIESCHE. 1999. Biological control
of Bemisia argentifolii (Hemiptera: Aleyrodidae) on poinsettia with inundative

















Hoddle & Van Driesche Control of Bemisia argentifolii 569

releases of Eretmocerus eremicus (Hymenoptera: Aphelinidae): does varying
the weekly release rate affect control? Bulletin of Entomological Research 89:
41-51.
HODDLE, M. S., AND R. G. VAN DRIESCHE. 1999. Evaluation of inundative releases of
Eretmocerus eremicus and Encarsia formosa Beltsville strain in commercial
greenhouses for control of Bemisia argentifolii on poinsettia stock plants. Jour-
nal of Economic Entomology vol. 92, 811-824.
LOPES, P. 1994. What's all the talk about Marathon? Floral Notes 7: 2-4.
O'NEIL, R. J., K. L. GILES, J. J. OBRUCJI, D. L. MAHR, J. C. LEGASPI, AND K. KATOVICH.
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PARRELLA, M. P. AND V. P. JONES. 1987. Development of integrated pest management
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PARRELLA, M. P., T. D. PAINE, J. A. BETHKE, K. L. ROBB, AND J. HALL. 1991. Evalua-
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PARRELLA, M. P., K. M. HEINZ, AND L. NUNNEY. 1992. Biological control through au-
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VAN DRIESCHE, R. G., S. M. LYON, M. S. HODDLE., S. ROY, AND J. P. SANDERSON.
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mercial poinsettia crops. Florida Entomol. 82: 570-594.
VAN DRIESCHE, R. G., M. S. HODDLE., S. M. LYON, AND J. P. SANDERSON. 1999b. Use
of insect growth regulators to reduce rates of Eretmocerus eremicus needed for
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Florida Entomologist 82(4)


December, 1999


ASSESSMENT OF COST AND PERFORMANCE OF
ERETMOCERUS EREMICUS (HYMENOPTERA: APHELINIDAE)
FOR WHITEFLY (HOMOPTERA: ALEYRODIDAE) CONTROL
IN COMMERCIAL POINSETTIA CROPS

R. G. VAN DRIESCHE', S. M. LYON', M. S. HODDLE1 2, S. ROY', AND J. P. SANDERSON3
1Department of Entomology, University of Massachusetts, Amherst, MA, 01003

2Current address: Department of Entomology, University of California,
Riverside, CA, 92521

3Department of Entomology, Cornell University, Ithaca, NY, 14853


ABSTRACT

Releases of Eretmocerus eremicus Rose and Zolnerowich (Hymenoptera: Aphelin-
idae) at release rates of 3.0-7.5 females per plant per week successfully suppressed
whitefly populations on commercial poinsettia (Euphorbia pulcherrima Willd. ex
Koltz.) crops in fall of 1996 at four Massachusetts commercial producers. At two sites,
the whitefly populations consisted exclusively of greenhouse whitefly, Trialeurodes
vaporariorum (Westwood), and at the other two sites exclusively of silverleaf whitefly,
Bemisia argentifolii Bellows and Perring. Parasitoids were received from commercial
suppliers and monitored weekly to determine the sex ratio of newly emerged adults,
as well as the rate of adult emergence. Commercially produced pupae were 48.1% (-
2.2 SE) female and had 58.1% (- 3.6 SE) emergence under greenhouse conditions.
Plants from the four biological control greenhouses in this trial at the time of sale of
the crop had an average of 0.55 (_ 0.28 SE) nymphs per leaf. Chemically-protected
poinsettias offered for sale at eight local retail outlets had an average of 0.16 (- 0.09
SE) nymphs per leaf. Final whitefly densities in both biological control and insecti-
cide-treated greenhouses were acceptable to consumers. An average of 6.8 insecticide
applications was applied to suppress whiteflies in chemical control greenhouses in
this trial, compared to 1.7 in the biological control greenhouses. Use of biological con-
trol was 27 fold more expensive, costing $2.14 per plant compared to $0.08 for chem-
ical control. Cost of biological control was inflated by three factors: (1) an incorrectly
high estimate by one grower of number of plants per greenhouse, (2) an unusually
long production period (23 weeks) for one grower, and (3) miscommunication with the
insectary concerning manner of filling orders to compensate for reduced percentage of
emergence of adult parasitoids from ordered parasitized nymphs. Control of these
cost-inflating factors would allow some reduction in the cost of the use of this parasi-
toid, but not to levels competitive with current pesticides. This study is the first to
demonstrate the ability ofE. eremicus releases to suppress T vaporariorum popula-
tions in commercial poinsettia crops and parasitism of T vaporariorum by E. eremicus
was 7.5-fold higher (ave. 24.8% parasitism of fourth instar nymphs in pooled seasonal
samples) than that observed in B. argentifolii (ave. 3.3%).

Key Words: Eretmocerus eremicus, Bemisia argentifolii, Trialeurodes vaporariorum
poinsettia, biological control, augmentative release, evaluation, cost, greenhouses

RESUME

Liberaciones de Eretmocerus eremicus Rose y Zolerowich (Hymenoptera: Aphelini-
dae) a raz6n de 3.0-7.5 hembras por plant por semana lograronun control efectivo de
mosquita blanca en cuatro cultivos comerciales de nochebuena (Euphorbia pulche-

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 571

rrima Willd. ex Koltz.) de Massachusetts durante el otofio de 1996. En dos sitios, las
poblaciones de mosquita blanca consistieron exclusivamente de la mosquita blanca de
invernadero, Trialeurodes uaporariorum (Westwood), mientras que en los otros dos si-
tios las poblaciones fueron exclusivamente de mosquita blanca de la hoja plateada,
Bemisia argentifolii Bellows and Perring. Los parasitoides fueron obtenidos de pro-
veedores comerciales y monitoreados semanalmente para determinar la proporci6n
de machos y hembras adults reci6n emergidos, asi como la tasa de emergencia de
adults. Las pupas producidas comercialmente fueron 48.1% (- 2.2 SE) hembras y tu-
vieron una tasa de emergencia de 58.1% (- 3.6 SE) bajo condiciones de invernadero.
Al moment de su venta, plants provenientes de los cuatro invernaderos de control
biol6gico usados en este studio tuvieron un promedio de 0.55 (- 0.28 SE) ninfas por
hoja. En comparaci6n, plants protegidas con insecticides tuvieron un promedio de
0.16 (- 0.09 SE) ninfas por hoja al moment de su venta en ocho locales comerciales.
Las densidades finales de mosquita blanca encontradas tanto en los invernaderos de
control biol6gico como en aquellos donde se emplearon insecticides fueron aceptables
a los consumidores. En promedio, 6.8 aplicaciones de insecticide fueron hechas para
controlar a la mosquita blanca en los invernaderos de control quimico usados en este
studio, comparado con 1.7 aplicaciones en los invernaderos de control biol6gico. El
costo del control biol6gico fue 27 veces mas caro que el del control quimico ($2.14 vs.
$0.08 por planta. El costo del control biol6gico result elevado debido a tres factors:
(1) el calculo err6neo (demasiado alto) por parte de un productor con respect al nu-
mero de plants por invernadero, (2) un period demasiado largo de producci6n (23 se-
manas) en el caso de un productor, y (3) falta de comunicaci6n con personal del
insectario respect a la manera de compensar el porcentaje reducido de emergencia de
adults parasitoides logrado por las ninfas parasitadas ordenadas. El costo del uso de
parasitoides podria reducirse al corregir los errors mencionados, pero no lo suficiente
para ser competitive con el uso de insecticides. Este studio es el primero en demos-
trar la eficacia del parasitoide E. eremicus en el control de T vaporariorum en cultivos
comerciales de nochebuena. El studio demostr6 que el parasitismo de T vaporario-
rum por E. eremicus fu6 7.5 veces mas alto que el obtenido con B. argentifolii (parasi-
tismo de 24.8% vs. 3.3% de ninfas de cuarto instar).




Silverleaf whitefly, Bemisia argentifolii Bellows and Perring, (= the "B" strain of
Bemisia tabaci [Gennadius]) and greenhouse whitefly, Trialeurodes uaporariorum
(Westwood), (both Homoptera: Aleyrodidae) are important pests of poinsettia (Eu-
phorbia pulcherrima Willd. ex Koltz.) in the United States (Helgesen & Tauber 1974,
Byrne et al. 1990, Bellows et al. 1994). The parasitoids most extensively used for
whitefly biological control in protected floricultural crops have been Encarsia formosa
Gahan and Eretmocerus eremicus Rose and Zolnerowich (formerly given as Eret-
m ocerus sp. 1. ...r. ir ..... I...I I. Hi, n...1.. '.1.. : I. A.'..'.l.IL' ) (Drost et al. 1996; Hod-
dle & Van Driesche 1996; Rose & Zolnerowich 1997; Hoddle et al. 1996, 1997ab,
1998abc; Hoddle & Van Driesche in press).
Previous trials in small, experimental greenhouses (holding 90 plants) suggested
that a Bemisia-adapted strain of E. formosa (referred to as the Beltsville strain, Heinz
& Parrella 1994) and E. eremicus had the potential to provide effective silverleaf
whitefly control in poinsettia crops if released at rates of 1-3 females per plant per
week (Hoddle et al. 1997ab, 1998a). Trials in commercial greenhouse poinsettia crops
in 1995 in Massachusetts compared the efficacy of E. eremicus and the Beltsville
strain of E. formosa at a release rate of 3 females per plant per week for each species.
In both summer stock plants and fall Christmas crop plants, E. eremicus suppressed
silverleaf whitefly better than the Beltsville strain of E. formosa (Hoddle and Van Dri-
esche, 1999). Poinsettias from these 1995 trials were sufficiently free of whiteflies to

















Florida Entomologist 82(4)


December, 1999


be acceptable to growers for use of cuttings from the summer crop (Hoddle & Van Dri-
esche, 1999) and sale to retailers in the Christmas poinsettia market in the fall (Hod-
dle and Van Driesche, in press).
Here we report further results from commercial trials conducted in fall 1996 in
Massachusetts in which four commercial poinsettia growers employed E. eremicus for
control of whiteflies. The purpose of the trial was to assess the robustness of E. ere-
micus releases as a means of suppressing whiteflies in commercial poinsettia crops
when applied to a wider variety of commercial conditions and when releases were
made by growers. At each of four commercial greenhouse ranges, we measured the
level of whitefly suppression achieved by releases ofE. eremicus compared to whitefly
populations treated chemically. At one study site, we made a further comparison to a
caged whitefly population not subject to either biological or chemical control. The
costs of biological control and chemical control were compared at all four locations.


MATERIALS AND METHODS

Study Sites and Experimental Design

The study was conducted at four commercial greenhouse growers. Two growers
were from the Connecticut River Valley in the western part of Massachusetts (Fair-
view Farms, Whately; Westover Greenhouses, Chicopee) and two were from eastern
Massachusetts (Loosigian Farms, Methuen; Konjoian Greenhouses, Andover). The
trial was conducted on the Christmas poinsettia crop between 3 July and 13 Decem-
ber 1996, with cropping periods varying from 17 to 23 weeks among sites. At each of
the four locations, weekly observations were made in two greenhouses, one managed
with biological control and one with insecticides. In the biological control green-
houses, our intent was to make weekly releases of 3 female E. eremicus per plant. In
the chemical control greenhouses, the growers managed pests with pesticides. At 3
sites (Loosigian, Konjoian, and Westover), growers ordered parasitoids directly from
commercial insectaries and made releases themselves. At one site (Fairview), we or-
dered and received parasitoids instead of the grower so we could assess the quality of
weekly shipments in terms of number of parasitoid pupae shipped (compared to num-
ber ordered) and sex ratio of emerging adult parasitoids. At this site, we made re-
leases and retrieved parasitoid exuviae weekly from release cups in greenhouses to
determine the percentage emergence under greenhouse conditions. Greenhouse di-
mensions, names of poinsettia cultivars grown, numbers of plants and potting ar-
rangements per greenhouse are given in Table 1. ("Plants" refers to independently
rooted poinsettias; pots may contain one or several plants.)
To formally demonstrate, at least at one site, that whitefly populations on poinset-
tia increase sharply if left uncontrolled, a control cage was installed in the biological
control greenhouse at Fairview Farms that received neither E. eremicus nor conven-
tional insecticides for whitefly management. The control cage (153 cm long by 92 cm
wide and 117 cm tall) was constructed of PVC pipe and covered with fine polyester
screening (95 micron dia openings) capable of excluding entrance of whiteflies and
parasitoids. The control cage contained 5 pots (20.3 cm), each with 3 poinsettia plants
(total, 15 plants per cage). To initialize the caged whitefly population, we inspected all
leaves on 100 plants from the greenhouse and chose plants that bore the number of
whitefly nymphs and pupae needed to match the density of the whitefly population in
the whole greenhouse as determined by a count of whiteflies on the potted cuttings at
the start of the trial (see Initial whitefly density). Because initial whitefly densities at
this site were very low, we augmented the silverleaf whitefly population in the biolog-





















TABLE 1. GREENHOUSE TYPE, SIZE, PLANT NUMBER, POT NUMBER, AND POINSETTIA CULTIVARS IN TRIAL.

# Plants in Cultivars
Site and treatment Type Dimensions greenhouse' # Pots in greenhouse and potting dates2


Fairview
biological control

Fairview chemical

Konjoian
biological control



Konjoian chemical


Loosigian
biological control
Loosigian chemical

Westover
biological control

Westover chemical


plastic hoop 5m x 30m 1500 8/15/96
1021 12/6/96
902 12/12/96
plastic hoop 5m x 30m 2448 for entire trial


glass




glass


10m x 42m 2550
3193
2818
1633
345


8/20/96
9/17/96
11/25/96
12/3/96
2/10/96


10m x 42m 3500 for entire trial


plastic hoop 7m x 48m 1243 for entire trial

plastic hoop 7m x 48m 1200 for entire trial


glass


glass


500 (21.6 cm); three plants each Freedom, 7 August


612 (25.4 cm); four plants each

625 (20.3 cm); three plants each;
1120 (15.2 cm); one plant each;
22 nine-plant hangers


Freedom, 7 August

Peter star, Freedom,
V-14, Supjibi, 20 August


800 (10.2 cm); 500 (14 cm); Peter star, Freedom,
2200 (15.2 cm); all one plant each V-14, Supjibi, 20 August


1243 (16.5 cm); one plant each

1200 (16.5 cm); one plant each


6m x 32m 2014 7/3/96 160 (20.3 cm); three plants each;
1331 12/4/96 256 ((30.5 cm); four plants each;
102 (38.1 cm); five plants each
15m x 61m 7800 for entire trial 2100 (17.8 cm); two plants each-
1200 (20.3 cm); three plants each


Red Sails, 13 August

Red Sails, 13 August

Supjibi, Maren, Monet,
V-17, V-14, Cortez Free-
dom, Peter Star, 3 July
Suiibi, Maren, Monet,
V-7, V-14, Cortez, Free-
dom, Peter Star, 3 July


'Earliest date gives initial number of plants. Pots were spaced initially at final densities. Subsequent dates reflect changes in number as crop was harvested.
Sources of cuttings variedbyvariety and grower: Westover Greenhouse propagated V-14 and V-17 varieties from stock plants and purchased others as rooted cuttings; Fairview Farm
purchased all plants as rooted cuttings; Loosigian Farms purchased unrooted cuttings; Konjolan Greenhouses propagated all varieties from stock plants.

















Florida Entomologist 82(4)


December, 1999


ical control greenhouse using silverleaf whitefly-infested plants produced by using
adult whiteflies from our laboratory colony of this species (see Whitefly augmenta-
tion). The numbers of whiteflies in the control cage were also augmented at the same
rate so that they had the same starting density as the biological control greenhouse.
While control cages were not installed at the other three trial sites, we have shown
in previous trials that silverleaf whitefly on poinsettia typically increases to high den-
sities if not controlled (Hoddle & Van Driesche 1996; Hoddle et al. 1997ab, 1998a). No
cage controls were included at sites that proved to be infested with greenhouse, rather
than silverleaf, whitefly. Consequently control data showing unrestricted growth for
that species in the absence of chemical or biological control were not collected in this
trial. However, such growth has been observed in other trials (Helgesen & Tauber
1974, Rumei 1982).
During the trial we collected data on (1) the weekly numbers released, percentage
emergence and sex ratio of E. eremicus, (2) the weekly whitefly densities in each
greenhouse, (3) the species of whitefly present at each grower, (4) insecticide usage
during crop production by each grower, and (5) the quality of plants at harvest (in
terms of whitefly infestation).


Crop Management

Source of cuttings, potting dates, spacing, plant removals. Three of four green-
houses potted cuttings between 7 and 20 August. One location (Westover Green-
houses) potted on 3 July in order to produce large ("tree") poinsettias. Table 1 provides
details on greenhouse type, size, numbers of plants, pot sizes, and cultivars.
Pesticide use. At three sites, the biological control greenhouse was treated only
with fungicides and plant growth regulators. At one site, Konjoian Greenhouses, in-
secticides were sprayed on 23-30% of the plants in the biological control greenhouse.
The infestation on these plants occurred because whitefly-infested plants from an-
other greenhouse on the property were placed directly beneath the intake vent of the
biological control greenhouse early in the cropping cycle, leading to a heavy, localized
infestation on benches near the air intake fans. Plants sprayed with insecticides were
excluded from sampling for the remainder of the trial.
Chemical and biological control greenhouses at all sites were treated with plant
growth regulators and fungicides. Names and application dates of insecticides used to
control foliar insects in chemical control greenhouses (and a portion of one biological
control greenhouse) are presented in Table 2.
Parasitoid releases. Biological control greenhouses at all four sites received weekly
releases ofE. eremicus for whitefly control. The intended weekly release rate was 3 fe-
male parasitoids per plant. When plants were removed from biological control green-
houses for sale, numbers of parasitoids released per greenhouse were reduced
accordingly. To avoid conflicts with parasitoids, yellow sticky cards (which are highly
attractive to E. eremicus, Sanderson, unpub. data), used by growers to monitor white-
flies and fungus gnats, were not placed in any of the biological control greenhouses.


Whitefly Species Composition, Initial Density Estimate, and Augmentation

Whitefly species. Both B. argentifolii and T. vaporariorum infest poinsettia in Mas-
sachusetts. To determine the whitefly species present in each test greenhouse, ten
heavily infested leaves were collected at each location in middle of the trial (mid-Oc-
tober). In the laboratory, all fourth instar nymphs, pupae and pupal cases were exam-
ined under a dissecting microscope and identified to species. Voucher specimens of























TABLE 2. APPLICATIONS OF INSECTICIDES MADE IN TRIAL FOR WHITEFLY CONTROL.

Greenhouse No. insecticide Insecticides applied Whitefly species Common
Grower type applications and application dates present in greenhouse chemical name

Fairview biocontrol 0 None B. argentifolii
Fairview chemical 1 Marathon 1%G (1% a.i.) (12 Sept.) B. argentifolii imidacloprid
Konjoian biocontrol 7 Thiodan 50WP (50% a.i.) (on 12 benches) T vaporariorum endosulfan
(19 Sept., 23 & 29 Oct.)'
Marathon 1%G (1% a.i.) (19 Sept., 6 Oct.)2 imidacloprid
Orthene PT 1300 DS (3% a.i.) acephate
(on 12 benches) (23 & 29 Oct.)'
Fulex Dithio (14% a.i.) (17 & 23 Nov.) sulfotep
Konjoian chemical 8 Thiodan 50WP (50% a.i.) (21 Aug. T vaporariorum endosulfan
& 12 Sept., 29 Oct., 10 Nov.)
Avid 0.15EC (1.9% a.i.) (21 Aug., 10 Nov.) abamectin
PT 1300 (3% a.i.) (12 Sept., 29 Oct.) acephate
Vydate L (20% a.i.) (24 Sept., 1 Oct.) oxymyl
Fulex Dithio (14% a.i.) (16 & 23 Nov.) sulfotep
Loosigian biocontrol 0 None T vaporariorum

Thlodan and Orthene were applied to 30% of the plants in the biological control greenhouse.
Marathon was applied to 23% of the plants in the biological control greenhouse.

























TABLE 2. (CONTINUED) APPLICATIONS OF INSECTICIDES MADE IN TRIAL FOR WHITEFLY CONTROL.

Greenhouse No. insecticide Insecticides applied Whitefly species Common
Grower type applications and application dates present in greenhouse chemical name

Loosigian chemical 8 Marathon 1%G (1% a.i.) (12 Sept.) T vaporariorum imidacloprid
Fulex Dithio (14% a.i.) (25 Sept., 17 & 21 sulfotep
Oct., 11 Nov.)
Fulex Nicotine (14% a.i.) (20 Nov.) nicotine
Fulex Thiodan (14% a.i.) (2 & 13 Dec.) endosulfan
Westover biocontrol 0 None B. argentifolii
Westover chemical 10 Azatin EC (3% a.i.) (9 & 16 Aug.) B. argentifolii azadirachtin
Tame 2.4EC (33.6% a.i.) (9 & 16 Aug.) fenpropathrin
Attain PT 1800 TR (0.5% a.i.) (11 Sept., bifenthrin
3 Oct.)
Preclude TR (4.8% a.i.) (17 & 26 Sept.) fenoxycarb
Marathon 1%G (1% a.i.) (4 Oct.) imidacloprid
Talstar (7.9% a.i.) (28 Oct., 1, 8 & 14 Nov.) bifenthrin
Enstar II (65.1% a.i.) (28 Oct., 1, 8 & 14 s-kinoprene
Nov)

Thlodan and Orthene were applied to 30% of the plants in the biological control greenhouse.
Marathon was applied to 23% of the plants in the biological control greenhouse.

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 577

whiteflies were not retained as no opportunity exists for taxonomic confusion in our
case. Trialeurodes vaporariorum is distinct in the context of greenhouse crops from all
other whiteflies, and all Bemisia whiteflies in poinsettia greenhouse crops in North
America are strain B of B. tabaci (= B. argentifolii), as the A strain was known only
from outdoor crops and even there has disappeared over the last decade in North
America, being replaced completely by the B strain.
Initial whitefly density. In order to determine if initial whitefly population densi-
ties in greenhouses designated as biological control greenhouses were within an ac-
ceptable range for management using parasitoids (considered by us to be 1.0 or fewer
live nymphs, pupae and adults combined per cutting, for B. argentifolii, based on lev-
els seen in our earlier trials, Hoddle et al. 1996, Hoddle and Van Driesche in press),
population densities were estimated on cuttings at the time of potting. At each loca-
tion, all nymphs, pupae, and adults on all leaves of 50 potted cuttings in the biological
control greenhouse were counted within 1-2 days of the potting date (see Table 1), and
numbers of leaves per cutting were recorded.
Whitefly augmentation. Because no whiteflies were seen on cuttings (n = 100) ex-
amined from the biological control greenhouse at one site (Fairview Farms), the
whitefly population there had to be augmented by introducing whitefly-infested
plants from our laboratory. Our intention was to add a number of immature whiteflies
sufficient to bring the per plant density at this site up to the average value of the three
other sites. To infest plants, we chose six uninfested poinsettia plants and used ven-
tilated, clip-on leaf cages (2.5 cm dia) to enclose 4-5 pairs of whitefly adults over leaves
for 2 days to produce eggs. We then counted the eggs produced and removed excess
numbers. Infested plants each had three infested leaves; each infested leaf (after egg
removal) bore an average of 105 B. argentifolii eggs (_ 8.6 SE, n = 10 leaves counted).
Infested plants were placed in the biological control greenhouse at Fairview Farms on
19 August. Initially, all infested leaf patches remained protected from attack by par-
asitoids within clip cages. One clip cage on each plant was removed on each of 19, 23,
and 29 August, allowing for a gradual introduction of the whiteflies into the crop. A to-
tal of 1890 eggs (6 plants x 3 patches x 105 eggs per patch) were added to this green-
house, which contained 1500 plants. We assumed 79% survival to the settled crawler
stage (based on cohort survival data in Hoddle et al. 1998a), giving a projected aug-
mented nymphal density of 1.0 nymph per plant, meeting our objective of a density
comparable to the average density of the other three biological control greenhouses in
the trial (1.05 nymphs per plant).

Parasitoid Sources, Application Methods, and Release Rates

The E. eremicus we used were purchased from commercial suppliers and shipped
as parasitized T vaporariorum fourth instar nymphs packed in sawdust, except for
the material used at Fairview Farms. Sawdust was omitted from shipments send to
our laboratory for use at this site in order to allow us to retrieve parasitized whiteflies
for estimation of parasitoid number per unit weight, sex ratio, and percentage emer-
gence. Over the course of the trial, parasitoids were obtained from two suppliers.
From the start of the trial until 4 October, parasitoids were supplied by Beneficial In-
sectary, Inc. (14751 Oak Run Rd., Oak Run, CA 96069). This colony was discontinued
mid-way through the trial, but the same population ofE. eremicus was available from
Koppert Biological Systems, Inc. in the Netherlands, and parasitoids from this source
were used to complete the trial. Koppert's production of this species was initiated with
the same material that had been used by Beneficial Insectaries (0. Minkenberg, pers.
comm.), so the genetic composition of the parasitoids used in the trial was consistent
throughout. Specimens from material sold by Koppert, Inc. as E. californicus (previ-

















Florida Entomologist 82(4)


December, 1999


ous name for E. eremicus) were submitted for taxonomic confirmation to Michael Rose
(specialist on the genera Eretmocerus and Encarsia, formerly of Texas A & M Univer-
sity) and were confirmed to be E. eremicus. Voucher specimens have been deposited in
the insect collection of the University of California, Riverside campus.
Parasitoid pupae were shipped directly to three of the four participating growers
because it was intended that processes used in the trial be as close to commercial as
possible. Therefore, at three locations growers received parasitoid shipments and
placed shipped material in release containers in greenhouses. These growers received
parasitized fourth instar T vaporariorum nymphs mixed with sawdust. This mixture
was placed in styrofoam release cups (6 cm tall, 5.5 cm wide at bottom, 8.5 cm wide
at top) that had the bottoms cut out and replaced with organdy (mesh 0.95 microns)
to allow for drainage. Cups were attached 10 cm above the canopy to wooden stakes
(50 cm long) placed in the potting media. In each biological control greenhouse, there
were 15 release cups distributed evenly throughout the crop. Each week, growers
emptied sawdust and any unemerged parasitoids from the previous week's release
into pots of plants on benches where cups were located and then added the new ma-
terial to the same cups. Watering was done so as to avoid wetting parasitoid pupae in
release cups (either drip irrigation was used or workers were advised not to wet saw-
dust in release cups when hand watering).
To estimate numbers of parasitoids released, parasitoids for use at Fairview
Farms were sent to our laboratory for subsampling before release. To estimate the
number of parasitoids released, we measured the number of pupae per unit weight of
material sent by the supplier, the weight of the shipment, the sex ratio of emerging
adults, and the percentage of pupae from which parasitoids successfully emerged un-
der greenhouse conditions.
Estimating number of E. eremicus pupae received from suppliers. Each week before
taking parasitoid pupae to Fairview Farms to be released, we counted the number of
live parasitoid pupae in each of ten 20 mg subsamples under a stereomicroscope at
25x. The average number of pupae per 20 mg was multiplied by 50 (to get the number
per gram) and then by the weight (in g) of all pupae received to determine the total
number of pupae actually shipped by the supplier in particular orders. The percent-
age deviation between this value and the number ordered was noted.
Estimating E. eremicus sex ratio. Each week, 200-300 parasitoid pupae from the
shipment sent to our laboratory were placed in a petri dish in a growth chamber at
22C and long day light regime (16:8 L:D) and held for emergence. One week after re-
ceipt, samples were frozen, and 15 groups of 10 adult parasitoids were examined at
50x with a stereomicroscope and their sex determined. Sexes were recognized based
on the clubbed antennae of the female (Rose & Zolnerowich 1997).
Estimating E. eremicus emergence rate. Each week before adding new parasitoid
pupae to release cups in the biological control greenhouse at Fairview Farm, whitefly
nymphs with parasitoid exit holes and remaining dead nymphs in cups from the pre-
vious week were retrieved and returned to the laboratory, frozen, and used to esti-
mate the parasitoid emergence rate. From the material returned to the laboratory
from each week of the trial, 15 samples of 10 parasitoid "pupae" (comprised of whitefly
nymphs containing dead parasitoid pupae and whitefly nymphal integuments with
parasitoid emergence holes) were examined at 25x under a stereomicroscope, and
classified as dead or emerged based on the presence of parasitoid emergence holes.
The percent emergence was calculated as the number of whitefly nymphs with para-
sitoid emergence holes divided by the total number examined (nymphs containing
dead parasitoid pupae plus whitefly nymphal integuments bearing parasitoid emer-
gence holes).

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 579

Calculating release rates ofE. eremicus. For one site (Fairview Farms) we used the
above information on number of parasitoid pupae per unit weight, together with sex
ratio and percent emergence, to adjust the number of parasitoid pupae actually re-
leased to achieve the intended release rate. At the other three sites, growers received
shipments directly and made their own releases, and quality control checks were not
made. At these sites, we estimated the number of parasitoid pupae that would be
needed to achieve our intended release rate (3 females per plant per wk) by assuming
a 50% female sex ratio and a 60% emergence rate. The sex ratio value was based on
advice from the supplier and the emergence rate was based on quality control checks
we made in greenhouse trials in 1995. Based on these assumptions, 10 parasitoid pu-
pae per plant per week were ordered for each participating grower, with exact num-
bers being calculated from numbers of plants in each biological control greenhouse.
Subsequent to the trial, we calculated the actual release rate achieved by reference to
quality control data collected from samples taken for the Fairview Farms site.

Whitefly Population Sampling

Densities of whitefly life stages (adult whiteflies, live and dead nymphs and pupae)
were estimated weekly throughout the cropping season by examining leaves on arbi-
trarily selected plants. At Westover Greenhouses, Konjoian Greenhouses, and Loosi-
gian Farms, two arbitrarily selected mature leaves from each of the upper and lower
halves of the plant from each of 30 arbitrarily selected plants (120 leaves total) in each
greenhouse were inspected for whiteflies on each sample date.
Numbers of leaves examined in the biological control greenhouse at Fairview
Farms differed from that of the other three sites because this greenhouse was also
part of a separate, concurrent experiment with a more intense level of sampling. At
Fairview Farms in the biological control greenhouse, three leaves (1 from the bottom
third of the plant, 1 middle, and 1 top) on 90 plants (270 leaves total) were inspected.
In the control cage in the biological control greenhouse at Fairview Farms, three
leaves on each of eight plants were inspected in a similar manner, weekly. At Fairview
Farms, the chemical control greenhouse was sampled for a shorter period than the bi-
ological control greenhouse. Three arbitrarily chosen leaves from each of 20 plants (60
leaves total) were inspected weekly, from 29 August to 13 November only. For figures
in which whitefly densities are plotted on log scales, 0.001 was added to all counts to
avoid zero values.

Measurement of Parasitoid-Caused Mortality

Whitefly nymphs killed by parasitoids through host feeding were included in
counts of dead nymphs or pupae made to estimate densities (see above). Deaths from
host feeding could not be distinguished from physiological death. Successful parasit-
ism was scored by noting numbers of visibly parasitized fourth instar whitefly
nymphs seen weekly on leaves on which whitefly stages were counted. Because para-
sitism was rare, weekly samples were not analyzed separately by date because of low
sample sizes. Instead, season-long rates of parasitism were computed for each of the
four biological control greenhouses by summing the number of visibly parasitized
fourth instar whitefly nymphs across all sample dates. Parasitism was computed as
the total number (A) of parasitized fourth instar whitefly nymphs summed across all
dates within one location, divided by this same value (A) plus the summed value in
the same samples of all whitefly pupae (B), (% parasitism = 100[A/ A +B]). Younger
whitefly stages (various nymphs) were not included in the estimation of parasitism,

















Florida Entomologist 82(4)


December, 1999


as these stages were too young for any parasitism they might have had to have be-
come visible in samples. Parasitism rates were compared statistically between the
combined samples of the two biological control greenhouses with T vaporariorum and
those of the two with B. argentifolii.

Whitefly Densities on Plants at Harvest

To compare the quality of plants in the trial to that of plants offered for sale in
Massachusetts, we determined the densities of live nymphs, pupae, and adults on
plants from the biological control and chemical control greenhouses and on poinsettia
plants at 8 retail outlets in Massachusetts in December 1996. Numbers of whiteflies
on plants at retail outlets were measured using a standardized market survey sam-
pling protocol used previously in Massachusetts, in which six leaves (2 bottom, 2 mid-
dle and 2 top) on 15 arbitrarily selected plants were examined for live whitefly
nymphs, pupae, or adults (Hoddle et al. 1997ab, 1998a).

Cost Analysis

To compare the costs of biological and chemical control, we computed the costs of
parasitoids versus pesticides used for whitefly control in the biological control and
chemical control greenhouses at each trial site. To compute the cost of chemical pest
control, grower spray records were examined and all applications of materials to sup-
press whiteflies were noted. Using 1995 catalog prices for insecticides and label appli-
cation rates and methods, we computed amounts and cost of insecticide applied in
each application. Seasonal expenditures for pesticides were then summed and divided
by the number of plants in each greenhouse to obtain a seasonal insecticide cost per
plant. To compute the cost of parasitoids we used the 1996 commercial price of $11 per
thousand pupae and an application rate of 10 pupae per plant (equal to 3 females per
plant, based on an assumed 50/50 sex ratio and 60% emergence rate). Costs of labor
for application were not considered for either chemicals or parasitoids (after Hoddle
& Van Driesche 1996).

Statistical Analyses

Average seasonal values of parasitoid emergence rate, sex ratio, and release rate
at Fairview Farms were compared to assumed or intended values with Student's t
test. Densities of whitefly nymphs were compared between chemical and biological
control greenhouses (and in one location, to whitefly nymphal densities in a control
cage) using nested ANOVAs. A Chi Square test was used to compare rates of parasit-
ism of greenhouse whitefly and silverleaf whitefly nymphs. This comparison was per-
formed on data after pooling across all sample dates for the pair of locations with each
whitefly species. A nested ANOVA was used to compare whitefly nymphal densities on
leaves from the biological control and chemical control greenhouses to whitefly densi-
ties on leaves of plants offered for sale at retail outlets.


RESULTS

Crop Management and Pesticide Use

In the chemical control greenhouses, from 1 to 10 insecticide applications were
made per greenhouse for whitefly control (avg. 6.8 + 1.8 SE, Table 2), with an ave. of

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 581

8 applications against T vaporariorum at two sites and 5.5 applications against B. ar-
gentifolii at the remaining two locations. In biological control greenhouses, three
growers used no insecticides and one made 7 applications to a portion (about 30%) of
the greenhouse (Table 2) to suppress whiteflies drawn in through the air intake vents.

Whitefly Species Composition, Initial Density, and Augmentation

Whitefly species. Of 216 nymphs and 404 pupal exuviae collected 17 October at
Loosigian Farms and of 798 nymphs and 242 pupal exuviae collected on the same date
at Konjoian Greenhouse, all were T. vaporariorum. In contrast, at Fairview Farms
and Westover Greenhouse, all fourth instar nymphs and pupae seen in samples dur-
ing the trial were B. argentifolii.
Initial whitefly density on potted cuttings. Mean numbers of live nymphs plus pu-
pae per leaf (_ SE) found in the initial count on poinsettia cuttings in the biological
control greenhouses varied from 0.0 to 1.6 (Fairview Farms [0.0 initially, 1.0 after
augmentation], Konjoian Greenhouses [1.6 + 0.7], Loosigian Farms [1.4 + 0.4], and
Westover Greenhouse [0.14 + 0.14]). Chemical control greenhouses at each site were
filled with cuttings from the same sources as the biological control greenhouses.
Silverleaf whitefly levels at two sites (Fairview Farms and Westover Greenhouses)
were considered suitable for use of biological control, based on previous trials in com-
mercial greenhouses in Massachusetts (Hoddle & Van Driesche, in press). Potential
for biological control of the greenhouse whitefly populations at Loosigian Farms and
Konjoian Greenhouses could not be evaluated because no previous trials on biological
control of this species on poinsettia had been run in Massachusetts.

Parasitoid Sex Ratio, Emergence, and Release Rates Achieved

Parasitoid sex ratio. The percentage of parasitoid pupae producing female parasi-
toids varied from 39 to 58% for 1500 insects examined from September to November
(Fig. 1). The seasonal average, 48.1% (+ 2.2 SE), did not differ statistically in a Stu-
dent's t test from the assumed value (50%) used in calculating numbers of pupae for
releases (t = -0.85, df = 9, P > 0.05)
Parasitoid emergence rate in greenhouse. The emergence rate in week one of the
trial at the monitored site (Fairview Farms) was very low (16%) for unknown reasons.
(Maximum daytime greenhouse temperatures were very high [36-43C], but so were
temperatures in several succeeding weeks in which emergence rates were higher.) In
weeks 2-17, emergence rates varied from 37 to 75% (Fig. 2). The average emergence
for weeks 2-17 was 60.7% (_ 2.6 SE). This value did not differ statistically in a Stu-
dent's t test from the assumed value (60%) used in calculating the release rate (t =
0.27, df= 15, P> 0.05).
Number of parasitoid pupae shipped by supplier versus number ordered. Important
discrepancies occurred between numbers of parasitoids ordered and numbers received.
At Fairview Farms, we calculated the number of parasitized nymphs to be placed in the
greenhouse weekly ourselves and corrected for this discrepancy. At the other three loca-
tions, the supplier sent higher numbers of parasitized nymphs than ordered. Counts in
our laboratory of numbers of parasitized nymphs averaged 264.6 ( 17.3 SE) per 20 mg
(range 144-388). For ten shipments, numbers of pupae received from Koppert Biological
Inc. were 201% of the number ordered (i.e., double), ranging from 127 to 365% of the de-
sired number. The main identifiable reason for this excess was compensation by the
supplier for non-emergence of, in their view, 30% of the shipped parasitoids. Subsequent
to this trial we learned that Koppert views emergence of its product to average 70% and
as a matter of policy, fills orders at 142% of the number requested to compensate.

















Florida Entomologist 82(4)


i


December, 1999











1


20-




13-Aug 23-Aug 2-Sep 12-Sep 22-Sep 2-Oct 12-Oct 22-Oct l-Nov 11-Nov 21-Nov 1-Dec 11-Dec
Date of Shipment

Fig. 1. Mean (_ SE) percentage female of adult Eretmocerus eremicus emerging in
the laboratory from material received weekly from insectaries supplying parasitoids
for release in trial.



Actual parasitoid release rates. Release rates achieved at study sites varied be-
cause actual numbers shipped differed from numbers ordered (see above) and be-
cause, for particular dates, actual sex ratios or percent emergence differed from
assumed values. At Fairview Farms, the average number of adult female parasitoids
actually emerging into the crop per plant per week from parasitized nymphs was 2.92
(_ 0.2 SE, range 0.60-4.15) (Table 3, Fig. 3). This rate did not differ statistically in a
Student's t test from the intended release rate of 3.0 females per plant per week (t =
-0.51, df= 1, P> 0.05).
Release rates at other greenhouses in the trial were estimated by using data on
sex ratio and percentage emergence derived from the parasitoids shipped to us for use
at Fairview Farms, and our estimate of the degree to which the supplier shipped more
parasitized nymphs than ordered (which were calculated based on the ratio of number
received to the number ordered for Fairview Farms). The supplier's over supply of par-
asitized nymphs to compensate for less than 100% emergence directly affected the re-
lease rate. Consequently, actual release rates (female parasitoid adults per plant per
week) were 6.67 (_ 0.87 SE) at Konjoian's Greenhouse, 4.47 (- 0.48 SE) at Loosigian
Farms, and 4.72 (_ 0.67 SE) at Westover Greenhouses.

Whitefly Population Monitoring

Fairview Farms. At Fairview Farms, only B. argentifolii was present. Whitefly
density in the control cage increased steadily over the course of the trial, reaching 19.0
(_ 4.6 SE) live nymphs per leaf by wk 18 (11 Dec.) (Fig. 4). Peak whitefly nymphal den-
sity in the control cage was 90 fold greater than that on uncaged plants in the biolog-
ical control greenhouse, which did not exceed 0.2 (_ 0.1 SE) nymphs per leaf (Fig. 5a).


582

100



80







a.
3 40'
s.

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 583

100 -



80
















0 ------ I Ii
13-Aug 23-Aug 2-Sep 12-Sep 22-Sep 2-ct 12-Oct 22-Oct -Nov 11-Nov 21-Nov 1-Dec 11-Dec
Date of Shipment

Fig. 2. Mean percentage (_ SE) emergence ofEretmocerus eremicus after one week
in the biological control greenhouse at Fairview Farms in Whately, MA.



Density of whitefly nymphs on uncaged plants in the biological control greenhouse
was similar to that observed in the chemical control greenhouse, in which plants were
treated with imidacloprid. Numbers of live pupae and adults were consistently below
0.04 per leaf(Fig 5 b, c).
Westover Greenhouses. At Westover Greenhouses, the grower produced a long sea-
son crop of extra large poinsettia plants that included poinsettia "trees" started 3 July
(6 weeks earlier than the normal mid-August starting date for smaller poinsettias).
The crop was infested exclusively with B. argentifolii and management problems in
the chemical control greenhouse occurred, leading to a whitefly outbreak that reached
86.3 (_ 20.8 SE) live nymphs per leaf on 3 October. Repeated applications of pesticides
(Table 2) reduced this population to 0.47 (_ 0.15 SE) nymphs per leaf by time of har-
vest (Fig. 6a).
In the biological control greenhouse, parasitoid releases consistently maintained
whitefly densities below 1 live nymph per leaf until 21 November, with numbers then
increasing to 1.31 (_D 0.26 SE) by the time of harvest (Fig. 6a). Densities of live whitefly
nymphs in the biological control greenhouse were consistently lower than those in
the chemical control greenhouse between 31 July and 13 November. Numbers of live
pupae and adults per leaf in the biological control greenhouse were consistently
lower than those observed in the chemical control greenhouse until 30 October
(Figs. 6 b, c).
Konjoian Greenhouses. At Konjoian Greenhouses, poinsettias were infested only
with T. vaporariorum. Numbers of live nymphs per leaf in the portion of the biological
control greenhouse not treated with insecticides exceeded 2 live nymphs per leaf on
one sample occasion (2.8 nymphs on 1 October), but were at acceptable densities (1.03
re 0.34 SE) at the time of sale (Fig. 7a).
0.34 SE) at the time of sale (Fig. 7a).























TABLE 3. QUALITY CONTROL INFORMATION USED IN ESTIMATING ACTUAL RELEASE RATE OF ERETMOCERUS EREMICUS AT FAIRVIEW FARMS BIO-
LOGICAL CONTROL GREENHOUSE.

No. No. No. Estimated release
% parasitized parasitized parasitized No. rate (females per
Release % female emergence nymphs/20 mg2 nymphs nymphs Ratio plants in plantper week)
date (X + SE) (X + SE) (X + SE) ordered received3 oversupplied greenhouse (X + SE)

16 Aug. 48 1' 17 + 3 144 14,895 11,232 0.75 1485 0
23 Aug. 48 1' 47 4 225 14,895 21,262 1.43 1485 0.80 0.14
30 Aug. 48 1' 69 + 3 185 14,895 15,078 1.01 1485 2.28 0.22
6 Sept. 58 + 3 57 3 219 14,895 16,717 1.12 1485 3.95 + 0.22
12 Sept. 56 3 70 3 200 14,895 15,100 1.01 1485 3.22 + 0.24
19 Sept. 42 + 4 75 3 293 14,895 27,982 1.88 1485 2.89 + 0.30
26 Sept. 57 3 73 4 176 14,895 17,688 1.19 1485 2.92 + 0.34
4 Oct. 43 + 5 65 + 4 351 16 14,895 55,650 3.73 1485 4.17 + 0.31
10 Oct. 44 + 3 70 + 3 354 18 14,895 28,276 1.90 1485 2.79 + 0.33
17 Oct. 42 + 5 49 + 4 275 13 14,895 32,175 2.16 1485 3.09 + 0.24
24 Oct. 50 + 5 59 + 5 373 8 14,895 31,752 2.13 1485 2.08 + 0.30
31 Oct. 48 1' 63 + 4 273 + 14 14,895 25,389 1.71 1485 2.94 0.35
7 Nov. 48 + 1' 37 + 4 234 + 12 14,895 18,954 1.27 1485 3.04 + 0.20
14 Nov. 48 + 1' 67 + 4 269 + 12 14,895 20,427 1.37 1485 1.81 0.21
21 Nov. 48 1' 55 + 3 388 + 16 14,895 33,026 2.22 1485 3.23 + 0.22

For indicated weeks, data on % of pupae that yielded females were not collected. To compute the estimate of the release rate, we used the seasonal average for proportion female.
For weeks 1-7, counts of pupae per 20 mg were supplied by the producer, with information on standard errors. For weeks 8-18, counts were made in our laboratory.
Pupae received were estimated as total weight of pupae received times number of pupae counted m 10 subsamples of 20 mg each, times 50 (see materials and methods for details).
4Pupae shipped in sawdust this week, so quality control data were not obtained.
Supplier changed as of 2 October.
































TABLE 3. (CONTINUED) QUALITY CONTROL INFORMATION USED IN ESTIMATING ACTUAL RELEASE RATE OF ERETMOCERUS EREMICUS AT FAIRVIEW
FARMS BIOLOGICAL CONTROL GREENHOUSE.

No. No. No. Estimated release
% parasitized parasitized parasitized No. rate (females per
Release % female emergence nymphs/20 mg2 nymphs nymphs Ratio plants in plant per week)
date (X + SE) (X + SE) (X + SE) ordered received3 oversupplied greenhouse (X + SE)

27 Nov. 50 + 4 54 + 4 282 + 7 14,895 29,134 1.96 1485 2.76 0.26.
5 Dec. 48 + 1' 63 + 04 259 + 14 14,895 24,815 1.67 1021 2.57 + 0.19
12 Dec. No data4 No data4 No data4 14,895 No data 902 No data4

For indicated weeks, data on % of pupae that yielded females were not collected. To compute the estimate of the release rate, we used the seasonal average for proportion female.
For weeks 1-7, counts of pupae per 20 mg were supplied by the producer, with information on standard errors. For weeks 8-18, counts were made in our laboratory.
Pupae received were estimated as total weight of pupae received times number of pupae counted m 10 subsamples of 20 mg each, times 50 (see materials and methods for details).
4Pupae shipped in sawdust this week, so quality control data were not obtained.
'Supplier changed as of 2 October.








0o
00
01

















Florida Entomologist 82(4)


December, 1999


4 -
C








13-Aug 23-Aug 2-Sep 12-Sep 22-Sep 2-Oct 12-Oct 22-Oct 1-Nov 11-Nov 21-Nov 1-Dec 11-Dec
Release date

Fig. 3. Estimated mean (_ SE) number of female Eretmocerus eremicus released
per plant in the biological control greenhouse at Fairview Farms. (See Table 3 for cal-
culations).


In the chemical control greenhouse, whitefly nymphal densities were similar to
those in the biological control greenhouse until 12 November. After 12 November,
nymphal densities remained lower in the chemical control greenhouse than in the bi-
ological control greenhouse through the end of the trial. Nymphal density was signif-
icantly lower in the chemical control greenhouse than in the biological control
greenhouse on the last sample date before harvest (df = 1, F = 6.91, P = 0.009) (Fig.
7a). Pupal and adult counts in the biological control greenhouse (Fig. 7b, c) were lower
than nymphal counts, but generally higher than counts of these stages in the chemi-
cal control greenhouse. Eight pesticide applications (Table 2) were made in the chem-
ical control greenhouse, which reduced whitefly densities to 0.13 ( 0.05 SE) live
nymphs per leaf at the time of sale (Fig. 7a).
Loosigian Farms. At Loosigian Farms, all whiteflies were T. vaporariorum. Num-
bers of live nymphs on the poinsettia crop in the biological control greenhouse ex-
ceeded 2 nymphs per leaf once, reaching 2.13 (_ 1.02 SE) on 10 September (Fig. 8a).
Densities of live nymphs on plants in the chemical control greenhouse reached 23.0
(_ 7.6 SE) per leaf on 17 September, and eight pesticide applications (see Table 2) re-
duced numbers to 2.68 (_ 1.0 SE), compared with 0.05 (_ 0.03 SE) in the biological con-
trol greenhouse (Fig. 8a), at time of harvest. Nymphal densities in the biological
control greenhouse were consistently lower than those in the chemical control green-
house from 17 September through the end of the trial. At harvest, density of nymphs
per leaf was significantly lower in the biological control greenhouse than in the chem-
ical control greenhouse (df = 1, F = 12.08, P = 0.0006).
Numbers of live pupae and adults per leaf in the biological control greenhouse
peaked at 0.08 (_ 0.05 SE) on 19 November and 0.11 (_ 0.05 SE) on 30 August, respec-
tively (Figs. 8b, c). In contrast, in the chemical control greenhouse, numbers of live pu-
pae reached 4.6 (_ 1.50 SE) (on 12 November) and of adult whiteflies, 0.96 ( 0.22 SE)
(on 15 October) (Figs. 8b, c).

















Van Driesche et al. Commercial Whitefly Biocontrol Trials 587


,1 -4.-I


L I ,
0.1



0.01'
/' I I i ,i


13-Aug 23-Aug 2-Sep 12-Sep 22-Sep 2-Oct 12-Oct 22-Oct 1-Nov 11-Nov 21-Nov
Sample Date


1-Dec 11-Dec 21-Dec


Fig. 4. Mean densities per leaf(_- SE) of live Bemisia argentifolii nymphs in control
cage at the biological control greenhouse at Fairview Farms.


Parasitoid-Caused Mortality
Numbers of dead nymphs on plants seen in whitefly density counts varied between
locations and treatments. At Fairview Farms, chemical control was highly effective in
suppressing whiteflies and dead nymphs were rarely detected. More dead nymphs
were observed in the biological control greenhouse at this site, but numbers remained
below 0.25 dead nymphs + pupae per leaf throughout the trial (Fig, 5d).
At Westover Greenhouses, where chemical control of whiteflies was ineffective un-
til near the end of the trial, counts of dead whitefly nymphs in the chemical control
greenhouse were high, exceeding 20 dead nymphs + pupae per leaf on some dates. In
contrast, at this site in the biological control greenhouse, whitefly densities remained
low and as a consequence, so did numbers of dead nymphs + pupae (Fig. 6d).
At Konjoian Greenhouses, numbers of live whitefly nymphs in the chemical and bi-
ological control greenhouses were similar on most sample dates (Fig. 7a), but numbers
of dead nymphs + pupae were greater in the biological control greenhouse (Fig. 7d).
At Loosigian Farms, where densities of live nymphs in the chemical control green-
house nearly always exceeded densities in the biological control greenhouse, so did
densities of dead nymphs + pupae (Fig. 8d).
Parasitism, while rare in all four biological control greenhouses, was significantly
higher (X2 = 22.27, corrected for continuity; df = 1; P < 0.005) in the two greenhouses
with T vaporariorum populations (31.3% of 32 whitefly stages at Loosigian Farms
and 18.4% of 228 whitefly stages at Konjoian Greenhouses) than at those locations
with B. argentifolii (6.7% of 150 whitefly stages at Westover Greenhouses and no par-
asitism observed, of 50 whitefly stages at Fairview Farms).

End-of-Crop Whitefly Densities
At sale, plants produced in biological control greenhouses in this trial had 0.55
(_ 0.28 SE) nymphs per leaf compared to 0.98 (_ 0.36 SE) for the chemical control


















588 Florida Entomologist 82(4) December, 1999

0.3 A
25 Biological Control House
0.25 -- Chemical Control House








S 0.15
0,05
0.0





15-Aug 25-Aug 4-Sep 14-Sep 24-Sep 4-Oct 14-Oct 24-Oct 3-Nov 13-Nov 23-Nov 3-Dec 13-Dec
0.15 -l




0.1
g.









s 0.05 t
C O





15-Aug 25-Aug 4-Sep 14-Sep 24-Sep 4-Oct 14-Oct 24-Oct 3-Nov 13-Nov 23-Nov 3-Dec 13-Dec





0.15









I- I
i *0.05+












Fig. 5. Mean densities per leaf( SE) at Fairview Farms greenhouses iin biological
15-Aug 25-A chemical control greenhouses o t 24-Oa t 3-Nov liilNov 23Nov 3s Dec 13Dec




houses at the test locations and 0.16 (D 0.09 SE) on poinsettias offered for sale at
: 0.25
0.2

0.15

0.05

15-Aug 25-Aug 4-Sep 14-Sep 24-Sep 4-Oct 14-Ot 24-Oct 3-Nov 13-Nov 23-Nov 3-Dec 13-Dec= 2, F =
Sample Date

Fig. 5. Mean densities per leaf (_- SE) at Fairview Farms greenhouses (in biological
control and chemical control greenhouses) of B. argentifolii live nymphs (A), pupae
(B), adults (C), and dead nymphs plus dead pupae (D).


houses at the test locations and 0.16 (_- 0.09 SE) on poinsettias offered for sale at
eight Massachusetts garden centers or shopping malls. A significant difference
among these three treatments was detected using a nested ANOVA (df = 2, F =
10.63, P = 0.0001). Tukey's Studentized Range test indicated that nymphal densi-
ties in the biological control greenhouses did not differ from those in either the
chemical control greenhouses in the test or the plants from retail outlets. However,


















Van Driesche et al. Commercial Whitefly Biocontrol Trials 589


10000 i
10000 T -0- Biological Control House
1000 -*-Chemical Control House A


|= 100 +



0.01
0.001 -- A 4 -4-I--- 4 ---4-----+ +--4-- I -t
10-Jul 24-Jul 7-Aug 21-Aug 4-Sep 18-Sep 2-Ocl 18-Oct 30-Oct 13-Nov 27-Nov 11-Dec



16-
14- B
0 12-
,. 10-
8-
>0. 6.
'J 4-
2-

10-Jul 24-Jul 7-Aug 21-Aug 4-Sep 18-Sep 2-Oct 16-Oct 30-Oct 13-Nov 27-Nov 11-Dec








4--
M- 2-- -

10-Jul 24-Jul 7-Aug 21-Aug 4-Sep 18-Sep 2-Odct 16-Oct 30-Oct 13-Nov 27-Nov 11-Dec


35 D

30

& 25
C-
,A 20
e.
E 15
z
| 10




10-Jul 24-Jul 7-Aug 21-Aug 4-Sep 18-Sep 2-Oct 16-Oct 30-Oct 13-Nov 27-Nov 11-Dec
Sample Date

Fig. 6. Mean densities per leaf (_ SE) at Westover Greenhouses (in biological con-
trol and chemical control greenhouses) of B argentifolii live nymphs (A), pupae (B),
adults (C), and dead nymphs plus dead pupae (D).




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