Download Density and Natural Enemies of the Asian Citrus Psyllid

Density and Natural Enemies of the Asian Citrus Psyllid,
Diaphorina citri (Hemiptera: Psyllidae), in the Residential
Landscape of Southern Florida1
Juang-Horng Chong,2,3 Amy L. Roda,4 and Catharine M. Mannion5
J. Agric. Urban Entomol. 27: 33–49 (2010)
ABSTRACT This study was conducted to determine the density, the
incidence of parasitism, and the generalist predator assemblage of the Asian
citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), on orange
jasmine plants [Murraya paniculata (L.) Jack] in the residential landscape of
Miami-Dade County, Florida. Flush shoots (10 cm) were collected from ten
orange jasmine hedges in each of the four communities (Doral, Coral Gables,
Palmetto Bay, and Homestead). We did not detect any consistent pattern in
the fluctuation of psyllid density over time in the four communities. The
greatest densities of eggs (65.5 6 36.3 eggs/shoot), early instars (first to third)
(87.2 6 47.8 nymphs/shoot), and late instars (fourth and fifth) (16.9 6 9.3
nymphs/shoot) were detected on 24 May 2006 in Palmetto Bay (egg) and Doral
(early and late instars). The density of adult psyllids remained below two
individuals per flush shoot at all locations for the entire sampling period.
There were no consistent correlations between environmental factors
(temperature, relative humidity, precipitation, and wind speed) and the
densities of nymphs and eggs. Percent parasitism by Tamarixia radiata
(Waterston) averaged 18.5% in 2006, and no consistent patterns were observed
among communities and sampling dates. Ladybeetles, syrphid flies, and
spiders were the most common generalist predators observed on the psyllidinfested flush shoots.
KEY WORDS
huanglongbing
Orange jasmine, invasive species, predator, parasitoid,
Asian citrus psyllid, Diaphorina citri Kuwayama, is one of the world’s most
serious pests of citrus production because it vectors the bacterium Candidatus
Liberibacter asiaticus, the causal agent of citrus greening disease (or huanglongbing) (Halbert & Manjunath 2004, Gottwald 2010). Diaphorina citri was first
detected in Palm Beach County, Florida in 1998 and has since spread to all citrusproducing counties in Florida (Halbert & Manjunath 2004). Currently, D. citri
1
Accepted for publication 21 July 2011.
University of Florida and USDA-APHIS, USDA-ARS Subtropical Horticulture Research Station,
Miami, FL 33158.
3
Corresponding author and current address: Department of Entomology, Soils and Plant Sciences,
Clemson University, Pee Dee Research & Education Center, 2200 Pocket Road, Florence, SC;
([email protected])
4
USDA-APHIS-PPQ-CPHST, Subtropical Horticulture Research Station, Miami, FL 33158.
5
University of Florida, Institute of Food and Agricultural Sciences, Tropical Research and Education
Center, Homestead, FL 33031.
2
33
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J. Agric. Urban Entomol. Vol. 27, (2010)
has been detected in Alabama, Arizona, California, Florida, Georgia, Hawaii,
Louisiana, Mississippi, South Carolina, and Texas (NAPIS 2011). The citrus
greening disease has been detected in Florida, Louisiana, and South Carolina
(NAPIS 2011).
Diaphorina citri feeds on many Citrus species and the related orange jasmine,
Murraya paniculata (L.) Jack (Rutaceae) (Tsai & Liu 2000), which are widely
planted in the residential landscape of southern Florida. Geographical distribution of D. citri closely follows that of the orange jasmine (Kohno et al. 2001).
Although developmental time was slightly longer, fecundity of D. citri on orange
jasmine plants was higher than on lime or mandarin (Nava et al. 2007). Orange
jasmine had been shown to serve as an inoculum reservoir (Damsteegt et al.
2010) and allows for transmission of Candidatus L. asiaticus to sweet orange by
the psyllids (Gasparoto et al. 2010). Therefore, orange jasmine may play an
important role in the epidemiology of the citrus greening disease as a host of D.
citri and an inoculum source for Candidatus L. asiaticus (Lopes et al. 2010).
Effective management of D. citri populations in the residential landscape can
reduce the risk of the spread of vector and disease. An understanding of the
population dynamics of D. citri should be an integral part of a management
program against the psyllid and the disease.
The seasonal abundance of D. citri had been studied in commercial citrus
groves and managed research plots (Tsai et al. 2000, 2002, Hall et al. 2008, Pluke
et al. 2008, Qureshi et al. 2009, Hall & Hentz 2011). Populations of adult D. citri
on orange jasmine plants increased in the summer and fall (Tsai et al. 2002) while
the psyllid was most abundant in citrus groves from May to July in Florida (Hall
et al. 2008) and in the spring in Puerto Rico (Pluke et al. 2008). Tsai et al. (2002),
Pluke et al. (2008), and Qureshi et al. (2009) reported that the abundance of D.
citri was correlated with the availability of newly flushed shoots, which are
essential for oviposition by adults and development of nymphs. Although
increases in D. citri population coincided with the flushing of citrus trees, psyllid
density in citrus groves of east-central Florida was dependent upon both the
availability of flushed shoots and environmental conditions, such as ambient
temperature and rainfall (Hall et al. 2008). The effect of pruning, which promotes
flushing on orange jasmine and citrus plants, on the population dynamics of D.
citri is unknown.
A classical biological control program was initiated in Florida soon after the
detection of D. citri with the goal of suppressing the psyllid populations. The
eulophid Tamarixia radiata (Waterston) and the encyrtid Diaphorencyrtus
aligarhensis (Shafee et al.) were released and established in Florida in 1999
(Hoy et al. 1999, Hoy & Nguyen 2001, Michaud 2004). Tamarixia radiata was
also unintentionally introduced into Puerto Rico (Pluke et al. 2008) and Texas (de
León & Sétamou 2010) with the spread of D. citri. Spiders, ladybeetles, syrphid
flies, and lacewings are major predators of D. citri (Michaud 2001, 2004, Michaud
& Olsen 2004, Pluke et al. 2005). The prevalence and impact of T. radiata and
other generalist predators on D. citri populations in the residential landscape is
unknown.
In this study, we surveyed for the density of D. citri, the incidence of
parasitism by T. radiata, and the general predator assemblages on orange
jasmine plants in four residential communities of Miami-Dade County, Florida.
The objectives of this survey were to elucidate patterns in the population
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
35
dynamics of D. citri and to provide a better understanding of the natural enemy
assemblage in residential landscapes. Results from this study provides
information on the influence of biological control factors on the population
dynamics of D. citri that may be useful in designing an integrated management
program against D. citri in the residential landscape.
Materials and Methods
Ten orange jasmine hedges were sampled biweekly from January to December
2006 to assess the density of D. citri in each of the residential communities or
cities (from south to north) of Homestead (25u289N, 80u289W), Palmetto Bay
(25u379N, 80u199W), Coral Gables (25u439N, 80u169W), and Doral (25u499N,
80u219W) in Miami-Dade County, Florida. The sampled hedges were between 1.0
and 2.5 m in height and 0.5 to 1.0 m in width. The hedges were about 1.6 km from
each other within the same community. The selected orange jasmine hedges were
planted as privacy fences on the property borders and were away from buildings
or not hidden under structures; therefore, they were fully exposed to the
surrounding environment.
On each sampling date, five 10-cm flush shoots (with a mixture of unfurled
and expanded but still tender leaves), grown between 0.5 and 1.0 m above ground
on the sides of each orange jasmine hedge, were randomly selected and collected.
The distance between collected shoots on an orange jasmine hedge was about 1 m.
The orange jasmine plants flushed continuously over the course of the study. All
sampled orange jasmine hedges were pruned at least once by homeowners or
landscape care contractors during the sampling period. Pruning removed all
shoots from the hedges but a large number of new shoots flushed within one week
of pruning. Collected shoots were placed into plastic bags and transported back to
the laboratory in iced coolers.
The collected shoots were examined under dissecting microscopes in the
laboratory at the USDA-ARS Subtropical Horticulture Research Station (SHRS),
Miami, Florida. The numbers of eggs, early (first to third) and late instars (fourth
and fifth), adults, and mummies were recorded for each shoot. The early instars
were distinguished by their smaller sizes and small or absent wing pads. The late
instars, which are the preferred hosts of T. radiata (Skelley & Hoy 2004), have
well-developed wing pads and red eyes. The mummies were separated into three
categories: those with round emergence holes on the thorax, those without
emergence holes, and those that had irregularly edged holes on the sides
(assumed to be the results of intraguild predation by generalist predators). The
arthropods found on the shoots were identified to family on site and the numbers
were recorded by the samplers. Aphids and coccinellids were identified to species
on site based on Halbert & Brown (2008) and Michaud et al. (2008), respectively.
Incidence of predation by any of the general predators observed over the course of
sampling was noted. Unfortunately, voucher specimens of the collected
arthropods were lost when the collection was moved from one location to another.
All shoots infested with nymphs of D. citri were kept for 14 days in plastic
containers (10 3 10 3 10 cm) for adult parasitoid emergence. The stems were
held in glass vials filled with tap water to maintain vigor.
Densities of eggs, early instars, late instars, and adults of D. citri at each
community were plotted against time. The proportion of parasitism was
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J. Agric. Urban Entomol. Vol. 27, (2010)
calculated as the number of emerged adult parasitoids divided by the sum of the
late instars and the mummies without emergence holes. The frequency of
observing individual generalist predator taxon was calculated from the total
observations of predators over the course of the sampling.
Daily average temperature, rainfall, relative humidity, and wind speed in each
community on each sampling date were obtained from nearby weather stations.
They were KMIA-Miami International Airport (25u479, 80u199) for Doral,
CW1733-South Miami (25u429, 80u209) for Coral Gables, DW5567-Palmetto Bay
(25u369, 80u209) for Palmetto Bay, and FAWN-Homestead (25u289N, 80u289W) for
Homestead. The weather stations were between 1 and 15 km from the sampled
hedges in each community. Correlation analyses were performed to assess the
reciprocal relationships among the psyllid density, the proportion of parasitism,
and the environmental factors (temperature, relative humidity, precipitation,
and wind speed) at a significance threshold of a 5 0.05 (PROC CORR; SAS
Institute 1999).
Results and Discussion
Density of Diaphorina citri. Diaphorina citri were present on all orange
jasmine hedges at four sampled communities in 2006. In Doral, there were five
peaks in the numbers of eggs per flush shoot: 1 February (29.0 6 9.6), 24 May
(34.1 6 16.2), 21 June (30.2 6 9.6), 30 August (30.3 6 16.5), and 20 December
(32.8 6 7.9) (Fig. 1). Density fluctuated between 1.0 6 0.4 and 17.4 6 6.4 eggs/
shoot for other sampling dates. The greatest density of early instars was 87.2 6
47.8 individuals/shoot (24 May) and remained below 22 individuals/shoot for the
rest of the year (Fig. 1). Except for 24 May (16.9 6 9.3) and 19 July (12.3 6 6.8),
the late instar density was below 10 individuals/shoot for the other sampling
dates (Fig. 1). The density of adults was below two adults/shoot for the entire
sampling period, with the highest densities on 1 February (1.2 6 0.5), 21 June
(1.3 6 0.5) and 19 July 2006 (1.3 6 0.6) (Fig. 1). There was another increase in
adult density at the end of the year (1.0 6 0.4 adults/shoot).
Densities were above 10 eggs/shoot on orange jasmine hedges in Coral Gables
on 1 February (19.9 6 8.1), 29 March (13.6 6 9.5), 24 May (11.6 6 6.7), and 8
November 2006 (17.5 6 8.2) (Fig. 2). The overall density of early instars was
lower than that in Doral, with a peak occurring on 12 April (23.0 6 19.7) (Fig. 2).
The density of late instars remained below five individuals/shoot except for 12
April (7.3 6 6.2) and 24 May (10.6 6 5.1) (Fig. 2). Adult density was below one
adult/shoot for most of the sampling dates except on 10 May (1.1 6 0.6) (Fig. 2).
In Palmetto Bay, the density of eggs was the greatest on 24 May (65.5 6 36.3),
followed by a lower density on 20 December (27.4 6 13.7), and remained below 20
eggs/shoot for the rest of sampling period (Fig. 3). Two peaks in the density of
early instars were identified on 6 January (34.9 6 10.1) and 26 April (28.6 6 17.5)
(Fig. 3). Except for 10 May, 24 May, and 25 October, the early instar density was
below five individuals/shoot in 2006. The overall density of late instars were
lower than that of early instars, with density of .5 individuals/shoots identified
on 6 January, 26 April, 19 July and 30 August (Fig. 3). The density of adults was
below two individuals/shoot, with the greatest densities on 15 March (1.2 6 1.0),
24 May (1.1 6 0.5), and 20 December (1.2 6 0.7) (Fig. 3).
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
37
Fig. 1. Mean (6SEM) density of eggs, early (first-third) instars, late (fourth and
fifth) instars, and adults of Diaphorina citri on 10-cm flush shoots of
orange jasmine plants in Doral, Miami-Dade County, FL in 2006.
Similar to Palmetto Bay, the density was less than 20 eggs/shoot in
Homestead, except on 1 March (43.2 6 24.0) and 24 May (21.4 6 9.9) (Fig. 4).
The greatest densities of early instars, late instars, and adults occurred on 1
March (33.0 6 23.0), 15 March (11.4 6 4.8), and 29 March (1.7 6 0.6), respectively
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J. Agric. Urban Entomol. Vol. 27, (2010)
Fig. 2. Mean (6SEM) density of eggs, early (first-third) instars, late (fourth and
fifth) instars, and adults of Diaphorina citri on 10-cm flush shoots of
orange jasmine plants in Coral Gables, Miami-Dade County, FL in 2006.
(Fig. 4). This was the only location where peak density of a more advanced
developmental stage lagged two weeks behind that of the previous stage. In
March, the average temperature was between 19.0 and 21.5uC (Fig. 5). At 25uC,
eggs hatched in 4.2 days and the total nymphal development was completed in
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
39
Fig. 3. Mean (6SEM) density of eggs, early (first-third) instars, late (fourth and
fifth) instars, and adults of Diaphorina citri on 10-cm flush shoots of
orange jasmine plants in Palmetto Bay, Miami-Dade County, FL in 2006.
12.8 days on orange jasmine (Tsai & Liu 2000). Nava et al. (2007) showed that at
24uC the developmental durations on orange jasmine were 3.6 and 14.1 days for
eggs and (total) nymphs, respectively. We assumed that there was one generation
in March and the peaks in density represented the numbers of individuals that
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J. Agric. Urban Entomol. Vol. 27, (2010)
Fig. 4. Mean (6SEM) density of eggs, early (first-third) instars, late (fourth and
fifth) instars, and adults of Diaphorina citri on 10-cm flush shoots of
orange jasmine plants in Homestead, Miami-Dade County, FL in 2006.
had completed successive developments. We estimated that the percent reduction
in D. citri density on field established orange jasmine hedges (due to all biotic and
abiotic causes and natural dispersal) was 23.6% for eggs, 65.4% for early instars,
and 85.1% for late instars. The percent reduction from eggs to adults was
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
41
Fig. 5. Average daily temperature, rainfall, relative humidity, and wind speed
recorded during the survey period in 2006.
estimated at 96.1%. To the best of our knowledge, the percent reduction in the
density of D. citri within a single generation has not been demonstrated on
orange jasmine. On citrus, 36–92% of nymphs disappeared from infested shoots
within 12 days due to freeze, predation, and parasitism (Qureshi & Stanly 2009).
Population dynamics of D. citri was studied in commercial citrus groves in
Florida and elsewhere (Hall et al. 2008, Pluke et al. 2008, Sétamou et al. 2008,
Qureshi et al. 2009) and on orange jasmine plants in Florida (Tsai et al. 2002).
There appeared to be a continuous migration of psyllids into the citrus groves in
east-central Florida (Hall & Hentz 2011). Psyllid density was the greatest in May,
June, and July in the citrus groves of east-central Florida (Hall et al. 2008).
Qureshi et al. (2009) reported greater adult psyllid density on citrus trees in
April-June in the eastern coastal region, May and July in the southwest region,
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J. Agric. Urban Entomol. Vol. 27, (2010)
and June, July, and September in the central region of Florida. Tsai et al. (2002)
reported five peaks in the number of adult psyllids (May, August, October,
November, and December). In this study, we did not observe consistent pattern in
the fluctuations of psyllid density (of all stages) among the sampling dates or
communities within a single county. We observed that the greatest density of
eggs and nymphs occurred on 24 May 2006 in several communities. Our short
sampling time (one year) might not be long enough to detect potential patterns in
the psyllid population dynamics.
In Miami-Dade County, daily temperature, rainfall, and relative humidity
(averaged across the four communities) were higher, and wind speed lower, in the
summer than other seasons (Fig. 5). It has been suggested that high rainfall and
wind may dislodged the adult psyllids from the plant (Aubert 1987) and also
promote the germination and growth of entomopathogenic fungi. We found that
the density of adults on orange jasmine plants was negatively correlated with
relative humidity (n 5 26, Pearson correlation coefficient, r 5 20.42407, P 5
0.0308) in Coral Gables, while it was positively correlated with relative humidity
(n 5 26, r 5 0.3924, P 5 0.0474) in Doral. The densities of eggs and nymphs were
not correlated to any of the environmental factors recorded in all sampled
communities. Michaud (2004) did not find any correlation between rainfall and
psyllid density. Tsai et al. (2002) observed a positive correlation between mean
population density and minimum temperature and rainfall. Hall et al. (2008)
were not able to correlate rainfall to flush abundance in citrus groves but found
positive correlations between temperature and psyllid density on young citrus
groves but not on old citrus groves.
The driving factor in D. citri phenology is the seasonal patterns of vegetative
growth of the psyllid’s host plants (Hall et al. 2008). Some studies suggested that
the influence of a particular weather condition on psyllid populations manifested
through the response of flushing pattern of host plants to the weather condition.
Tsai et al. (2002) suggested that the positive correlation between psyllid density
and rainfall was the result of the growth of new shoots of orange jasmine
promoted by a higher rainfall. Observing positive correlation between temperature and psyllid density in young citrus groves, Hall et al. (2008) suggested that
young citrus groves flushed continuously, thus allowed the psyllid population to
grow over a wide range of temperatures. High temperature and rainfall, as well
as pruning, may also have the same stimulating effects on the density of new
flush shoots on orange jasmine in our study. However, we were not able to make
the connection between environmental factor, maintenance practice, flush shoot
density, and psyllid density because we did not record the density of flush shoots.
Natural enemies of Diaphorina citri. Biweekly average percent parasitism varied from 0 to 57% among the sampled communities and dates (Fig. 6). In
Doral, the highest percent parasitism was recorded on 15 March (53.2 6 27.4%),
followed by 8 November (52.3 6 18.4%). In Coral Gables, the highest percent
parasitism was on 8 November (51.8 6 16.6%), followed by 27 September (50.8 6
20.6%) and 20 December (50.0 6 25.0%). Percent parasitism exceeded 50% in
Homestead only on 1 February (57.0 6 25.0%). Average percent parasitism was
always below 50% in Palmetto Bay. When averaged across sampling locations
and dates, the percent parasitism of D. citri by T. radiata in the residential
landscape of Miami-Dade County was 18.5%. No correlations were found between
percent parasitism and any of the environmental factors recorded.
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
43
Fig. 6. Mean (6SEM) percent parasitism of Diaphorina citri by the parasitoid
Tamarixia radiata on 10-cm flush shoots of orange jasmine plants in four
communities in Miami-Dade County, FL in 2006.
Tsai et al. (2002) reported less than 1% parasitism and few predators on
orange jasmine plots and citrus trees, and they concluded that natural enemies
were not important in regulating the populations of D. citri. In commercial citrus
groves, Michaud (2004) reported parasitism rates of only 0.2–1.3%, and suggested
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J. Agric. Urban Entomol. Vol. 27, (2010)
that generalist predators, particularly the ladybeetles, had greater impacts. In
contrast, Pluke et al. (2008) reported parasitism rates of 70–100% in citrus groves
and 48–77% in orange jasmine plants in Puerto Rico. Qureshi et al. (2009)
reported that the percent parasitism in commercial citrus groves of Florida
averaged less than 20% in the spring and summer but could reach as high as 56%
in November, which appeared to be similar to the results from this study.
However, we caution making direct comparison between our study and others
because the methods in estimating percent parasitism or incidence of parasitism
vary from one study to the next. Results from this study suggest that T. radiata
was an important mortality factor for D. citri populations in urban landscapes
although the exact impact of parasitism on psyllid abundance may vary according
to seasons and locations.
Michaud (2004) suggested that the low parasitism rate in citrus groves might
be due to intraguild predation by ladybeetles. In this study, we detected only two
mummies with clear sign of intraguild predation (i.e., chew mark on the sides)
(out of 1304 samples). No hyperparasitism was observed in our survey. Based on
the rare incidence of intraguild predation and hyperparasitism, it may be
tempting to suggest that both factors were not the main causes of parasitoid
mortality. Our sampling method did not account for the predation of parasitized
but yet mummified psyllid nymphs, which was often shown to be preferred by the
intraguild predators (e.g., Chong & Oetting 2007). Intraguild predation of young
nymphs often does not leave behind any telltale signs as the nymphs were
completely consumed or the cadavers eventually fall off the plant. In addition,
intraguild predation by predators with sucking mouthparts does not leave behind
clearly visible feeding marks on the cadavers. It was not known if adult
parasitoids were consumed or their foraging activities interfered by any of the
generalist predators reported in this study. Therefore, this study did not
document the full extent of intraguild predation on T. radiata. A better
understanding of the impacts of intraguild predation is important to assessing
and enhancing the performance of T. radiata in the field.
In the residential landscape of Miami-Dade County, the most common
predators foraging on psyllid-infested orange jasmine hedges were the coccinellids, particularly the multicolored Asian ladybeetle, Harmonia axyridis Pallas,
which was observed on 5% (all life stages combined) of the orange jasmine shoots
examined (Table 1). A large number of H. axyridis larvae had been observed in
this study to feed on both D. citri and the brown citrus aphid, Toxoptera citricida
(Kirkaldy) (Hemiptera: Aphididae). Another commonly encountered generalist
predator on D. citri-infested shoots was the larvae of syrphid flies but predation
of D. citri nymphs by syrphid fly larvae was not observed. Eggs of lacewings were
found at most locations but the larvae were only observed infrequently at Doral.
Various species of spiders were active in orange jasmine hedges and predation of
D. citri adults was occasionally observed. We observed a large number of longlegged flies (Diptera: Dolichopodidae) aggregated at infested hedges and these
predatory flies were observed to capture and consume adult D. citri in the air.
Various species of ants of the genera Crematogaster, Pheidole, Pseudomyrmex,
and Solenopsis were also observed. Except for Pseudomyrmex, all ants were
attracted by the copious amount of honeydew produced by the psyllid nymphs
and the aphids, and were observed to actively collect the honeydew. Nymphs of
Anthocoridae were observed to feed on young psyllid nymphs on two occasions.
Neuroptera
Hymenoptera
Hemiptera
Diptera
Aranea
Acari
Coleoptera
Order
Dolichopodidae
Anthocoridae
Reduviidae
Formicidae (Crematogaster,
Pheidole, Pseudomyrmex and
Solenopsis spp.)
Chrysopidae
Syrphidae
Cycloneda sanguinea
Curinus coeruleus
Unidentified sp.
Chilocorus stigma
Coccinellidae
Harmonia axyridis
Family/species
Egg
Larva
Larva
Pupa
Adult
Larva
Pupa
Adult
Adult
Adult
Egg
Larva
Egg
Larva
Pupa
Adult
Adult
Nymph
Nymph
Adult
Adult, nymph
Adult, nymph
Life stage
0.2
0.0
3.9
0.4
0.1
0.3
0.3
0.5
0.3
0.0
0.0
0.1
0.0
0.0
0.0
0.0
0.0
0.1
0.0
0.1
1.4
0.2
Palmetto Bay
0.0
0.0
2.7
0.2
0.2
0.3
0.2
0.0
0.1
0.0
0.0
0.2
0.0
0.0
0.0
0.2
0.0
0.0
0.0
0.0
1.8
0.1
Homestead
0.2
0.1
3.2
0.4
0.2
0.2
0.2
0.0
0.0
0.2
0.0
0.4
0.0
0.0
0.1
0.0
0.1
0.0
0.1
0.0
1.0
0.2
Doral
Sampled community
0.0
0.0
2.5
0.6
0.2
0.0
0.0
0.0
0.0
0.0
0.2
0.1
0.1
0.1
0.0
0.1
0.0
0.0
0.0
0.0
1.3
0.0
Coral Gables
Table 1. Frequency (in % of total samples collected) of generalist predators associated with orange jasmine hedges
infested with Diaphorina citri in Miami-Dade County, Florida in 2006.
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
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J. Agric. Urban Entomol. Vol. 27, (2010)
Direct predation by nymphs of Reduviidae was never observed. A large number of
spiders and few mites (not identified) were also collected. Majority of the spiders
collected in this study were of the family Salticidae. Michaud (2004) collected a
hunting spider Hibana velox (Becker) (Araneae: Anyphaenida) in Florida citrus
groves, while Qureshi & Stansly (2009) did not report on the identity of the
spiders collected in their study. The impacts of predation on the psyllid
populations in this study were unknown.
Michaud (2004) reported H. velox, seven species of coccinellids, at least two
species of lacewings, one species of syrphid fly, and T. radiata as major mortality
factors of D. citri. Michaud (2002) also observed active attacks of D. citri by
spiders (Anyphaenidae, Clubionidae, Oxyopidae, and Salticidae), lacewings
(Chrysopidae and Hemerobiidae), hoverflies (Syrphidae), and predatory bugs
(Anthocoridae). The most common coccinellid species in citrus groves of central
Florida were Cycloneda sanguinea L., H. axyridis, and Olla v-nigrum Mulsant
(Michaud 2004). Qureshi & Stansly (2009) observed spiders, lacewings (Ceraeochrysa sp. and Chrysoperla sp.), ants, syrphid flies, anthocorids, mirids, the
Asian cockroach (Blattella asahinai Mizukubo), and four ladybeetle species [C.
sanguinea, Curinus coeruleus (Mulsant), O. v-nigrum, and H. axyridis], with the
ladybeetles being the most abundant. Pluke et al. (2005) recorded Coelophora
inaequalis F. and C. sanguinea as the most common ladybeetle species in Puerto
Rico. Harmonia axyridis was not collected by Pluke et al. (2005). The assemblage
of generalist predators collected in this study was similar to but the frequency
lower than that in commercial citrus groves as reported by Michaud (2004) and
Qureshi & Stansly (2009). The most common predators associated with D. citri
infested orange jasmine hedges in the residential landscape of southern Florida
were H. axyridis, followed by Chilocorus stigma (Say). Few C. sanguinea and C.
coeruleus, and no O. v-nigrum, were collected in this study.
Predators and ants may not be directly attracted to D. citri but by the large
aphid populations that were also established on the sampled orange jasmine
(Michaud & Browning 1999). We do not know of any instance in which
infestations of brown citrus aphids had caused significant damage and aesthetic
concerns to orange jasmine plants grown in the residential landscape. The
establishment of an aphid colony on the orange jasmine hedges could serve to
increase predation of D. citri by attracting a large number of generalist predators.
Diaphorina citri is a suitable prey for the ladybeetles C. coeruleus, C. sanguinea
L., Exochomus childreni Mulsant, H. axyridis and O. v-nigrum (Michaud & Olsen
2004). Olla v-nigrum showed significant numerical response to the psyllid
populations (Michaud 2001). Qureshi & Stansly (2009) demonstrated that where
insecticide applications were restricted, ladybeetles can be a major mortality
factor in psyllid populations. Therefore, practices to preserve ladybeetles may
help enhance predation levels on psyllid and aphid populations on orange jasmine
plants and citrus trees in residential landscapes.
Aubert (1987) suggested that entomopathogenic diseases maybe the most
important mortality factor of D. citri. However, Halbert & Manjunath (2002)
suggested that the disease of D. citri may be rare in Florida. Diaphorina citri was
known to be infected by Isaria (5Paecilomyces) fumosoroseus (Wize) Brown &
Smith and Hirsutella citriformis Speare in Indonesia (Subandiyah et al. 2000)
and Florida (Meyer et al. 2007, 2008, Hoy et al. 2010). We did not observe any
diseased D. citri in our survey.
CHONG et al.: Asian citrus psyllid in residential landscape of southern Florida
47
In summary, we did not observe consistent patterns in the population
dynamics of D. citri on orange jasmine hedges in residential communities of
southern Florida. Wind speed, rainfall, relative humidity and ambient temperature did not appear to correlate to psyllid density, except for the density of
adults. Such a lack of general pattern may hamper the development of a
predictive tool for psyllid density and may present a significant challenge to the
formulation of an accurately timed management program.
With a lack of predictive tools, pest managers may have to use other
monitoring methods to determine the abundance of D. citri on citrus trees and
orange jasmine plants. The flushing patterns of citrus trees are dictated by
seasonality and cultural maintenance and have been shown to correlate
positively with adult density (Qureshi et al. 2009). Therefore, chemical
management of D. citri had to be adjusted according to the flushing pattern of
citrus trees. A predictive model of flushing pattern of citrus may aid the timing of
insecticide applications (Hall et al. 2008). Other monitoring methods and
sampling plans, such as sticky card (Hall 2009, Hall & Hentz 2010, Hall et al.
2010), stem-tapping sampling (Hall et al. 2007, Hall & Hentz 2010), and flush
shoot sampling (Hall & Albrigo 2007, Sétamou et al. 2008), are being developed.
Geospatial analysis has also been used to predict the dispersal of psyllids and the
spread of disease (Costa et al. 2010, Leal et al. 2010).
The parasitoid T. radiata played an equally important role in suppressing the
D. citri population in the residential landscape as in the commercial citrus groves
(Qureshi et al. 2009). The average parasitism rate was low (14–28%), and was not
likely influenced by disease, hyperparasitism or intraguild predation. The impact
of generalist predators on D. citri populations, which had been shown to be
important in citrus groves (Qureshi & Stansly 2009), deserves a more thorough
assessment on residential orange jasmine hedges and citrus trees.
Acknowledgments
We want to thank Luis Bradshaw and Roger Coe of University of Florida, and Jeffrey
Tefel of USDA-ARS-SHRS, for their technical assistance. Francis Reay-Jones (Clemson
University) and four anonymous reviewers provided helpful comments to earlier drafts of
the manuscript. This study is supported by a cooperative agreement between USDAAPHIS-PPQ Eastern Region and the University of Florida awarded to C. Mannion.
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