Effect of Zelus longipes (Hemiptera: Reduviidae) on Diap

citri (Hemiptera: Liviidae) and Its Parasitoid Tamarixia ra

(Hymenoptera: Eulophidae) under Controlled Conditions

Authors: Bernardo Navarrete, Daniel Carrillo, Ana Y. Reyes-Martinez, S

Sanchez-Peña, Jose Lopez-Arroyo, et. al.

Source: Florida Entomologist, 97(4) : 1537-1543

Published By: Florida Entomological Society

URL: https://doi.org/10.1653/024.097.0428

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 Navrette et al.: Predation of Diaphorina citri and Tamarixia radiata by Zelus longipes 1537

EFFECT OF ZELUS LONGIPES (HEMIPTERA: REDUVIIDAE) ON

DIAPHORINA CITRI (HEMIPTERA: LIVIIDAE) AND ITS PARASITOID
TAMARIXIA RADIATA (HYMENOPTERA: EULOPHIDAE) UNDER
CONTROLLED CONDITIONS

BERNARDO NAVARRETE1,*, DANIEL CARRILLO2, ANA Y. REYES-MARTINEZ3, SERGIO SANCHEZ-PEÑA3,

JOSE LOPEZ-ARROYO4, HEATHER MCAUSLANE5 AND JORGE E PEÑA2
1
Instituto Nacional de Investigaciones Agropecuarias, Estación Experimental Tropical Pichilingue, Ecuador

2
University of Florida, Tropical Research and Education Center, Homestead, FL 33031, USA

3
Universidad Autónoma Agraria Antonio Narro, Saltillo Coahuila, Mexico

4
INIFAP, Campo Experimental General Terán, Carretera Montemorelos-China Km 31, General Terán C.P. 67413,
Nuevo León, Mexico

5
University of Florida, Department of Entomology and Nematology, Gainesville, FL 32611, USA

*Corresponding author; E-mail: [email protected]

ABSTRACT

Studies were conducted under controlled laboratory conditions to evaluate the effect of the
predator, Zelus longipes (Hemiptera: Reduviidae) on mortality of Diaphorina citri (Hemip-
tera: Liviidae) as well as its effect on the specialized parasitoid, Tamarixia radiata (Hyme-
noptera: Eulophidae). All tested life stages of Z. longipes consumed significantly more D.
citri adults than nymphs. Zelus longipes nymphs were only effective as predators of D. citri
adults at a predator density of 8 individuals (or specimens) per arena. The mortality of D.
citri nymphs caused by Z. longipes adult females was higher at the densities of 2 or more
predators per arena. All densities of male and female adult Z. longipes resulted in mortality
of nearly all the T. radiata adult parasitoids offered. The importance of intraguild predation
and possible interference with T. radiata are discussed.

Key Words: citrus psyllid, intraguild predation, functional response, assassin bug,
Murraya

RESUMEN

Se estudió bajo condiciones de laboratorio el efecto del depredador Zelus longipes (Hemip-
tera: Reduviidae) sobre el psílido de los cítricos Diaphorina citri (Hemiptera: Liviidae), así
como su efecto sobre el parasitoide Tamarixia radiata (Hymenoptera: Eulophidae). Todos los
estadios de Z. longipes consumieron una cantidad significativamente más alta de adultos
que de ninfas de D. citri. Las ninfas de Z. longipes fueron efectivas solamente como depre-
dadores de adultos de D. citri, cuando la densidad del depredador era de 8 ninfas por arena
experimental. Todas las densidades de machos y hembras de Z. longipes consumieron todos
los adultos del parasitoide T. radiata. Se discute la importancia de depredación intragre-
mial.

Palabras Clave: psilido de los cítricos , depredación intragremial, respuesta funcional, chin-
che asesina, Murraya

The ubiquity and importance of intra-guild al. (1993) concluded that in aphidophagous sys-
predation has been considered in numerous sys- tems, the addition of generalist predators such as
tems involving predators, parasitoids and patho- Zelus renardi Kolenati (Hemiptera: Reduviidae)
gens (Lucas 2005). Predators and parasitoids, and Nabis spp. (Hemiptera: Nabidae) generated
serving as intra-guild prey, may be attacked by sufficient mortality of the predator Chrysoperla
other generalist predators, pathogens and para- carnea (Stephens) (Neuroptera: Chrysopidae) to
sitoids (Lucas 2005). For instance, Rosenheim et negatively affect population regulation of the in-

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 1538 Florida Entomologist 97(4) December 2014

tended prey, Aphis gossypii (Glover) (Hemiptera: MATERIALS AND METHODS

Aphididae).
The psyllidophagous system of Diaphorina citri Plant Material and Experimental Arenas
Kuwayama (Hemiptera: Liviidae) in Florida’s cul-
tivated Rutaceae (i.e., Citrus, Murraya) may also Murraya exotica (formerly known as M. pa-
demonstrate the phenomenon of intra-guild preda- niculata), which is grown as an ornamental
tion (Michaud 2004). Intra-guild predation on im- hedge in Florida, and is a host of D. citri was
mature stages of the introduced parasitoid Tamar- used in all experiments. Murraya exotica plants
ixia radiata (Waterson) (Hymenoptera: Eulophidae) were grown in 3.8-L plastic pots with potting me-
in Florida citrus groves resulted in > 95% mortality dia (pine bark, 60% + Canadian sphagnum peat
of the parasitoid, thereby reducing the efficacy of and vermiculite). The plants were placed inside
this biological control agent against D. citri. 91.4 × 61 cm screen cages (mesh size 1 mm2) and
A component of this psyllidophagous system is kept inside a greenhouse to avoid unwanted ar-
the assassin bug, Zelus longipes (L.) (Hemiptera: thropod infestations. Experimental arenas were
Reduviidae: Harpactorinae), a generalist predator constructed by cutting M. exotica flushes free of
(Kalsi & Seal 2011) of D. citri (Peña et al. 2008). any damage, leaving a 5-cm stem to hold the cut-
The abundance of Z. longipes on Rutaceous plants ting firmly upright when formed into bouquets
has been verified in the field. For example, Z. lon- with exposed leaves. Bouquets were formed by
gipes was reported preying upon D. citri on citrus inserting the stems into a 26-mL vial (polysty-
in central and central-east Florida (Michaud 2002; rene, measuring 26 × 51 mm with snap-on caps,
Hall et al. 2008) and in Murraya exotica L. (for- Fisherbrand® cat. # 03-338-3c) filled with 20
merly M. paniculata) in south Florida (Peña et al. mL water and a small hole in the cap. The bou-
2008). Zelus longipes was observed eating adults of quets were placed inside wide-mouth mason jars
T. radiata on an 80-m-long M. exotica hedge during (Ball®, 946 cm3 volume) with a fine screen (0.25
observation periods from 10:00 till 11:00 and from mm2) mesh lid and a piece of wet cotton inside
13:00 till 14:00 each day over a period of 4 consecu- to provide moisture. All experiments were con-
tive weeks (Peña et al. 2008). Numbers of Z. lon- ducted in an insectary at the Tropical Research
gipes recorded did not differ during morning and and Education Center (TREC), in Homestead,
afternoon hours. The mean density of Z. longipes Florida under 25 ± 2 °C, 12:12 h L:D and 65 ±
throughout the study ranged from 7.8 to 24.3 per 2% RH, unless stated otherwise.
30 min of observations while the number of D. citri
adults /flush fluctuated between 0.15 and 4.95. Pe- Insect Colonies
na (unpubl. 2009) recorded 0 to 12 D. citri adults,
0 to 52 eggs, and 0 to 62 nymphs/flush in a 20-m- A 30 m long × 1 m tall unsprayed M. exotica
long M. exotica hedge. During the same study, he hedge located at TREC that had a long term in-
recorded from 1 to 66 Z. longipes during a 2-min festation with D. citri was the source of insects.
walk conducted 3 times a day around a 10-m-long Adult D. citri were collected with an aspirator
portion of the same M. exotica hedge. Additionally, and nymphs were collected by cutting infested
Z. longipes activity was surveyed every other day flushes.
during 4 weeks for 1 h at 8:00, 11:00 and 16:00 Zelus longipes adults of both sexes were col-
during the spring of 2011 (AYRM, unpubl. data). A lected from the M. exotica hedge with a paint-
total of 1677 individuals were observed, resting or brush and placed inside plexiglass cages (30 × 30
preying on D. citri, but also preying on other natu- × 30 cm) with 200 cm2 of corrugated cardboard
ral enemies such as the parasitoid T. radiata and that served as oviposition substrate. Honey was
the predator Hippodamia convergens Guérin-Mén- supplied on 2 pieces of paper (5 × 5 cm) affixed to
eville (Coccinellidae). During surveys on M. exotica the cage walls. Water was provided in a clear plas-
of predator activity and density in the spring and tic container, with a cotton roll inserted through
summer of 2012, Z. longipes was recorded as the the container lid to serve as a wick. After 2 days
most frequent predator, and was observed feeding of oviposition the corrugated cardboard with the
on D. citri and also on coccinellids, tachinid flies, eggs was transferred to a new cage. Zelus longipes
and small wasps, such as T. radiata (BN, unpubl. first instars emerged approximately15 days later.
data). These nymphs were fed daily with live Drosophila
Clearly there are abundant anecdotal observa- spp. (Diptera: Drosophilidae) adults (1-3 flies per
tions to indicate that Z. longipes is an abundant individual) until the 4th instar. Fourth instar Z.
predator with the potential to reduce D. citri pop- longipes were fed daily with adults of Anastrepha
ulation suppression through intra-guild preda- suspensa (Loew) (Diptera: Tephritidae) (1-3 flies
tion. To supplement those observations, here we per individual), which were supplied by the Divi-
present studies conducted under controlled condi- sion of Plant Industry, Biocontrol Rearing Facil-
tions to evaluate the possible effect of Z. longipes ity, Florida Department of Agriculture and Con-
on D. citri and on the specialized parasitoid, T. sumer Services, Gainesville, Florida. Drosophila
radiata. spp. was reared using ripe banana fruits kept in

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 Navrette et al.: Predation of Diaphorina citri and Tamarixia radiata by Zelus longipes 1539

1-L plastic containers and flies were transferred GLM (SAS 2001). Tukey’s test was used to de-
to the Z. longipes cages using an aspirator. In this termine significant differences between means
rearing system, Z. longipes adults were obtained (P < 0.05). The number of D. citri eggs was not
45 to 60 days after the emergence of the 1st in- normally distributed (PROC GPLOT, SAS 2001)
stars. All predators were deprived of food for 24 h so a 3(x+1) transformation was used to normal-
prior to initiating the experiments. ize the data.
Tamarixia radiata were collected on the M.
exotica hedge and then placed with M. exotica
flushes infested with D. citri 4th and 5th instars. Functional Response of Zelus longipes to Diaphorina
Psyllid infested flushes were formed into large citri Adults
bouquets inserted in polystyrene containers (26
× 51 mm, Fisherbrand®) and then placed inside Six densities of D. citri adults (presumably
a plexiglas cage (30 × 30 × 30 cm). Then, 20 T. mated, 1:1 么:乆) (4, 8, 12, 16, 20, and 24 indi-
radiata adults were introduced to the cages for viduals per arena) were offered to a single 1-d-
4 days. After the oviposition period, flushes with old Z. longipes, presumably mated female adult.
presumably parasitized D. citri nymphs were Both the prey and the predator were placed in
transferred to emergence cages where parasitoids the glass jar experimental arena with 1 flush
began to emerge approximately 12-15 days later. of M. exotica. Twenty four h later, the numbers
Honey and water were provided in the same way of live and dead adults of D. citri were counted.
as for Z. longipes. This procedure was repeated Each prey density was replicated 6 times. The
every 10 days. untreated control for each density consisted
of the prey without the predator. The type of
functional response was determined using the
Susceptibility of Different Psyllid Life Stages to polynomial logistic regression model (Juliano
Predation by Zelus longipes 2001) analyzed in SAS (SAS Institute 2001).
Experimental arenas (glass mason jars with Ne exp(P0 + P1N0 _ P2N20 +P3N30)
volume of 946 cm3) were prepared with either 2 =
M. exotica flushes and 20 adults of D. citri (pre- N0 2 3
1 + exp(P0 + P1N0 _ P2N 0 +P3N 0)
sumably mated, 1:1 么:乆) or 1 flush of M. exotica
and 20 D. citri 5th instars. Sets of 1, 2, 4 or 8 1-d- Where Ne is the number of prey eaten, No is
old unfed Z. longipes adults (么 and 乆 tested sepa- the initial number of prey, and P0, P1, P2, and P3
rately), or 1st instars of Z. longipes were intro- are parameters estimated in the model.
duced into the arenas. Experimental arenas with The handling time and attack constant were
D. citri but no predators were used as a control. estimated using the NLIN procedure (Juliano
Twenty four h after introducing the predators, the 2001) with the Hassell equation as a model (Has-
flushes were inspected under a stereomicroscope sell 1978):
and the number of D. citri eggs, dead D. citri and Ne = N0{1 - exp[-aT N0/(1 + bN0 +aThN20]}
Z. longipes per flush were counted. Each preda-
tor-stage density was replicated 5 times. In this equation, a is the attack constant, b is
a constant, Th is handling time and T is total time
Susceptibility of Tamaraxia radiata Adults to Predation available for Z. longipes to search for and attack
by Zelus longipes the D. citri adults.

Experimental arenas were prepared with 2 M. Prey Preference of Zelus longipes

exotica flushes and 20 1-d-old T. radiata adults
(1:1 么:乆). Sets of 1, 2, 4 or 8 1-d-old unfed Z. lon- Prey preferences of 1st instar nymphs, adult
gipes adults (么 or 乆), or 1, 2, 4, 8, or 12 1st instars females or males of Z. longipes, were determined
of Z. longipes were introduced into the arenas. by choice tests. The prey species offered were T.
Twenty four h later, the number of live and dead radiata, D. citri, and A. suspensa adults. In the
adults of both predator and prey was counted. The first choice test, one flush of M. exotica containing
untreated control was set up in the same way but 15 adults of D. citri and 15 adults of T. radiata
contained no Z. longipes. The response variables was introduced into the experimental arena fol-
were the number of dead T. radiata adults and lowed by the introduction of a 1st instar, an adult
number of surviving Z. longipes. Each predator male, or an adult female Z. longipes. The arena
density was replicated 5 times. was sealed thereafter. Twenty four h later, the
numbers of live and dead adults of D. citri and
Statistical Analysis T. radiata were counted. Each experimental unit
was replicated 15 times. The ` index proposed
The response variables were analyzed us- by Manly et al. (1972) was used to quantify prey
ing analysis of variance performed with PROC preference.

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 1540 Florida Entomologist 97(4) December 2014

Zelus longipes adults at densities of 2 to 8 pred-

ln(Ne ) ators per arena caused significantly higher mor-
N tality (females: F = 117.58; df = 4, 20; P < 0.001;
_=
ln(N'e) males: F = 28.77; df = 4, 20; P < 0.001) of D. citri
N' adults than did a single male or female (Table 1).
However, the average number of prey consumed
1 per adult predator decreased significantly when
`=
(1 + a) the number of predators in the arenas increased
(females: F = 83.62; df = 4, 20; P < 0.001; males: F
Where N and N’ are the numbers of each pro- = 8.65; df = 4, 20; P < 0.001) (Table 1).
vided prey type and Ne and Ne’ are the numbers Zelus longipes nymphs were only effective as
of each prey type killed. The preference ` index predators of D. citri adults at a predator density
assigns values from 0 to 1, where 0.5 represents of 8 per arena (F = 14.04; df = 4, 20; P<0.001). The
no preference. Mean ` values were considered sig- number of prey consumed per Z. longipes nymph
nificant when 95% confidence intervals based on was higher when a single predator was released in
the t-distribution did not overlap with ` = 0.5. the arena compared with 2, 4 and 8 predators per
The same methodology was used for a separate arena, which caused low mortality similar to that
experiment in which adult Z. longipes (male and observed in the predator-free control (Table 1).
female) had to choose between 15 adults of A. sus- The mortality levels of D. citri nymphs caused
pensa and 15 adults of D. citri. by Z. longipes adult females were density de-
pendent. Mortality was significantly higher at
RESULTS a predator density of 8 females/arena, followed
by 4 or 2 females/arena, and 1 female/arena; the
Susceptibility of Different Psyllid Stages to Predation latter showed mortality rates similar to the con-
by Zelus longipes trol treatment (F =30.44; df = 4, 20; P < 0.001)
(Table 1). The average number of D. citri nymphs
All tested stages of Z. longipes consumed sig- consumed per Z. longipes female did not vary
nificantly more D. citri adults than nymphs (F = among the tested predator densities (Table 1).
77.05; df = 1, 149; P < 0.001). In addition, adult Four to 8 Z. longipes males per arena caused
female and male Z. longipes showed significantly the highest number of dead D. citri nymphs com-
higher predation rates on D. citri than did 1st in- pared with the results obtained at lower predator
star Z. longipes (F = 11.68; df = 2, 147; P < 0.001). densities or in the untreated control (F =13.17; df

TABLE 1. MEAN NUMBERS (± SEM) OF DIAPHORINA CITRI ADULTS AND NYMPHS FOUND DEAD IN TREATMENTS WITH
DIFFERENT DENSITIES OF ZELUS LONGIPES ADULT FEMALES, ADULT MALES OR 1ST INSTARS.

D. citri adults D. citri nymphs

Predator No. D. citri No. D. citri No. D. citri No. D. citri No. D. citri
Zelus Stage density prey dead killed/ predator dead killed/ predator
Adult female 0 20 0.2 ± 0.2 c 0.0 ± 0.0 d 0.2 ± 0.2 d 0 ± 0.0 b
1 20 14.8 ± 1.4 b 14.8 ± 1.4 a 1.2 ± 0.2 cd 1.2 ± 0.2 a
2 20 18.6 ± 0.7 a 9.3 ± 0.3 b 2.0 ± 0.3 bc 1.0 ± 0.2 a
4 20 18.0 ± 0.5 a 4.5 ± 0.1 c 3.2 ± 0.7 b 0.8 ± 0.2 a
8 20 19.8 ± 0.2 a 2.5 ± 0.02 cd 6.0 ± 0.3 a 0.8 ± 0.04 a

Adult male 0 20 0.2 ± 0.2 c 0 ± 0.0 b 0.4 ± 0.2 c 0 ± 0.0 b

1 20 8.4 ± 2.7 b 8.4 ± 2.7 a 1.0 ± 0.5 bc 1.0 ± 0.5 ab
2 20 16.2 ± 1.5 a 8.1 ± 0.7 a 3.0 ± 0.3 ab 1.5 ± 0.2 a
4 20 18.8 ± 0.8 a 4.7 ± 0.2 ab 4.2 ± 0.9 a 1.0 ± 0.2 ab
8 20 18.6 ± 1.7 a 2.3 ± 0.1 b 5.0 ± 0.4 a 0.6 ± 0.1 ab

1st Instar nymph 0 20 0.4 ± 0.2 b 0 ± 0.0 b 0.0 ± 0.0 b 0 ± 0.0 c

1 20 2.4 ± 0.7 b 2.4 ± 0.7 a 1.8 ± 0.2 ab 1.8 ± 0.2 a
2 20 2.0 ± 0.8 b 1.0 ± 0.4 ab 1.4 ± 0.4 ab 0.7 ± 0.2 b
4 20 3.0 ± 1.1 b 0.8 ± 0.3 ab 2.2 ± 0.5 ab 0.6 ± 0.1 cb
8 20 8.6 ± 1.0 a 1.0 ± 0.1 ab 3.4 ± 1.2 a 0.4 ± 0.2 cb

Means followed by different letters within columns separated by lines differ significantly (Tukey’s test, P < 0.005).

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 Navrette et al.: Predation of Diaphorina citri and Tamarixia radiata by Zelus longipes 1541

= 4, 20; P < 0.001). The average number of D. citri

nymphs consumed per Z. longipes male was sig-
nificantly higher than the control when 2 preda-
tors were released per arena (F = 4.13; df = 4, 20;
P < 0.01) (Table 1).
Compared to the control, only the treatment
with 8 Z. longipes nymphs could reduce signifi-
cantly the number of D. citri nymphs (F = 3.82; df
= 4, 20; P < 0.01). The number of prey consumed
per Z. longipes nymph was density dependent.
The average number of D. citri nymphs consumed
per Z. longipes nymph was significantly higher
when 1 predator was released per arena and it
decreased as the number of predators increased
(F = 18.83; df = 4, 20; P < 0.01) (Table 1).

Susceptibility of Tamarixia radiata Adults to Predation

by Zelus longipes

All densities of male (F = 93.98; df = 4, 20; P

< 0.001) and female (F = 318.71; df = 4, 20; P <
0.001) Z. longipes adults resulted in approximate-
ly 90% mortality of the parasitoids offered com-
pared to the untreated control (< 1%). Mortality
of the adult parasitoids increased with increasing
densities of Z. longipes nymphs. Densities as low
as 2 nymphs per arena significantly increased T.
radiata mortality relative to natural mortality
(control) (F = 28.77; df = 4, 20; P = <0.001) (Fig. 1).

Functional Response of Zelus longipes to Diaphorina

citri Adults

The regression analysis resulted in the follow-

ing coefficient estimates: intercept (a) = -1.1742 ±
1.57 (SE), r2 = 0.56, P = 0.4545; linear (b) = 0.8682
± 0.4106 (SE), r2 = 4.47, P = 0.003; quadratic (c)
= -0.0621 ± 0.0304 (SE), r2 = 4.17, P = 0.041 and Fig. 1. Number of Tamaraxia radiata adults found
cubic (d) = 0.00125 ± 0.00067 (SE), r2 = 3.45, P = dead in treatments with different densities of Zelus lon-
0.0631. The linear coefficient (b) was > 0 indicat- gipes adult females (A), adult males (B), and 1st instar
ing that adult female Z. longipes showed a Type nymphs (C). Treatments with different letters are sig-
nificantly different (Tukey’s test, P < 0.05). Error bars
III functional response (Juliano 2001). The model
represent one standard error of the mean.
produced the following values for the parameters
of the Hassel equation: The handling time (Th)
was 1.15 ± 0.08 h and the attack rate constant (a) DISCUSSION
was 0.017 ± 0.004 (Fig. 2).
Our research suggests that Z. longipes can
Prey Preference of Z. longipes reduce the population of D. citri in M. exotica.
Females were slightly more efficient predators
First instar Z. longipes nymphs expressed a of D. citri adults than are males, which may be
significant preference for T. radiata adults (95% explained by the fact that Z. longipes females
confidence intervals did not include ` = 0.5) over are larger and perhaps need more prey than the
D. citri adults. Neither male nor female adults of males (Kalsi 2011). Due to their small size, 1st
Z. longipes showed a preference for one prey type instar nymphs of Z. longipes were not able to re-
over the other (Fig. 4). In the second experiment duce psyllid numbers to the same extent as the
Z. longipes females showed a significant pref- adults; Groups of 2 or 3 Z. longipes nymphs of-
erence for A. suspensa adults (95% confidence ten attacked a single prey, and thus an individual
intervals did not include ` = 0.5) over D. citri nymph consumed fewer psyllids than did an indi-
adults, but males did not show any preference vidual adult Z. longipes. Similar results were not-
(Fig. 3). ed with Zelus exsanguis Stål attacking Ephestia

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 1542 Florida Entomologist 97(4) December 2014

Fig. 2. Functional response of single adult females of

Z. longipes that were provided with increasing densities
of D. citri adults. Data fit a Type III functional response.

kuehniella Zeller and Drosophila spp. (Edwards

1966).
Immatures and adults of Z. longipes consumed
relatively fewer 5th instars of D. citri than adult D.
citri. Apparently Z. longipes prefers to eat mobile
prey instead of sessile prey. Visual stimuli seem
to be the most important cue needed for reduviids
to trigger an attack, as shown in work with Z.
renardii and Rhynocoris marginatus Fab. (Hari-
dass et al. 1988; Cisneros & Rosenheim 1998). In
contrast, other Harpactorinae like Scipinia repax Fig. 3. Preferences of Zelus longipes 1st instar
Stål and Nagusta sp., which are specialist preda- nymphs, adult males and females of Z. longipes between
tors of spiders, seem to rely on other sensory cues Diaphorina citri and Tamarixia radiata adults (upper
for orienting to prey (Jackson et al. 2010). Tama- panel) and Diaphorina citri and Anastrepha suspensa
rixia radiata adults were suitable prey for adults adults (lower panel). The preference index ` assigns
and nymphs of Z. longipes, suggesting the pos- preference values from 0 to 1, where 0.5 represents no
sibility that intra-guild predation may be disrup- preference. The position of ` in the bottom (0 < ` < 0.5)
tive to biological control of the psyllid. This may or top (0.5 < ` < 1) of the graph shows preference for a
particular prey. Mean `-values were considered signifi-
also explain low levels of parasitism at certain cant when 95% confidence intervals (error bars) based
sites (Peña et al. 2008). Kalsi & Seal (2011) men- on the t-distribution did not overlap with ` = 0.5.
tioned that Z. longipes can be a predator of other
natural enemies like Orius spp. Zelus renardii
has been reported as an important predator of tional responses for the same predator species
parasitoids of the genus Aphytis, thus interfer- may be explained by the use of different prey with
ing with biological control of the California red different behaviors and size.
scale Aonidiella aurantii (Maskell) (Heimpel et As generalist predators, reduviids are thought
al. 1997). No cannibalistic behavior was observed not to express strong prey preferences (Louis
among Z. longipes individuals during any experi- 1974). Our work confirms that Z. longipes adults
ment, likely as a result of the short duration (24 do not exhibit a preference for D. citri versus T.
h) of trials. According to personal observations by radiata as prey items. However, Z. longipes 1st
BN of the Z. longipes colony, cannibalism will be- instar nymphs prefer T. radiata adults over D.
gin after 3 d of starvation. Similar behavior was citri adults, which may be due to the compara-
observed by Evans (1976) with the pirate bug An- tively smaller size of the parasitoid. For instance,
thocoris confusus (Reuter). Cogni et al. (2002) inferred from choice experi-
Zelus longipes female adults had a type III ments that Z. longipes adults prefer smaller prey.
functional response to D. citri adults (Juliano In this study, adult females of Z. longipes showed
2001). Type III functional response is typical for a prey preference for A. suspensa adults over D.
generalist predators that can switch from one citri adults; in this case the females chose a bigger
prey to another (Hassell 1978; Akre & Johnson prey, which may be explained by greater nutri-
1979; van Baalen et al. 2001). Kalsi (2011) found tional needs of the females or by their bigger size
that both genders of Z. longipes adults had a type in comparison with males.
II functional response when feeding upon flies of Our research indicated that Z. longipes adults
the genus Euxesta. The different types of func- could potentially prey upon adults of D. citri un-

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 Navrette et al.: Predation of Diaphorina citri and Tamarixia radiata by Zelus longipes 1543

der field conditions. Considering the high popula- Fabricius (Harpactorinae-Reduviidae-Heteroptera-

tions of this reduviid seen in south Florida, this Insecta). Proc. Indian Acad. Sci. Sect. B 97: 41-48.
predator may contribute to D. citri mortality. HASSELL, M. P. 1978. The dynamics of arthropod pred-
However, it was also demonstrated in this re- ator-prey systems. Princeton University Press, New
Jersey.
search that the parasitoid T. radiata is a suitable HEIMPEL, G. E., ROSENHEIM, J. A., AND MANGEL, M.
prey for Z. longipes. The prey preference studies 1997. Predation on adult Aphytis parasitoids in the
showed that 1st instar nymphs had a preference field. Oecologia 110: 346-352.
for the smaller parasitoid over the larger D. citri. JACKSON, R. R., SALM, K., AND NELSON, X. J. 2010. Spe-
Hence, the real effect of this predator on parasit- cialized prey selection behavior of two East African
oids and other natural enemies should be tested assassin bugs, Scipinnia repax and Nagusta sp. that
under field conditions, particularly in M. exotica prey on social jumping spiders. J. Insect Sci. 10: 1-19.
systems where Z. longipes appears to be more fre- JULIANO, S. A. 2001. Non-linear curve fitting: predation
quent than on Citrus spp. and functional response curves, pp. 178-196 In S. M.
Schener and J. Gurevitch [eds.], Design and analysis
of ecological experiments. Oxford Univ. Press, New
York, NY.
ACKNOWLEDGMENTS KALSI, M. 2011. Potential predators of corn-infesting
picture-winged flies (Diptera: Ulidiidae) in Home-
We thank K. Santos and A. Vargas for their help.
stead, Florida: seasonal abundance, distribution
We thank Drs. K. Wyckhuys (CIAT, Vietnam), J. Jacas
and functional response. M.S. Thesis, Univ. Florida,
(Universitat Jaume I, Spain) for their suggestions to im-
Gainesville.
prove this manuscript. This research was supported by
KALSI, M., AND SEAL, D. R. 2011. Milkweed assassin bug
INIAP (Ecuador) and INIFAP (Mexico).
(suggested common name) Zelus longipes L. (Insecta:
Hemiptera: Reduviidae). (http://entnemdept.ifas.ufl.
edu/creatures/beneficial/bugs/zelus_longipes.htm)
REFERENCES CITED LOUIS, D. 1974. Biology of Reduviidae of cocoa farms in
Ghana. American Midl. Nat. 91: 68-89.
AKRE, B. G., AND JOHNSON, D. M. 1979. Switching and LUCAS, E. 2005. Intraguild predation among aphidopha-
sigmoid functional response curves by damselfly na- gous predators. European. J. Entomol. 102: 351-354.
iads with alternative prey available. J. Anim. Ecol. MANLY, B., MILLER, P., AND COOK, L. 1972. Analysis of a
48: 703-720. selective predation experiment. American Nat. 106:
CISNEROS, J. J., AND ROSENHEIM, J. A. 1998. Changes 719-736.
in the foraging behavior, within-plant vertical dis- MICHAUD, J. 2002. Biological control of Asian citrus
tribution, and microhabitat selection of a generalist psyllid, Diaphorina citri (Hemiptera: Psyllidae) in
insect predator: an age analysis. Environ. Entomol. Florida: a preliminary report. Entomol. News 113:
27: 949-957. 216-216.
COGNI, R., FREITAS, A. V. L., AND AMARAL FILHO, B. F. MICHAUD, J. 2004. Natural mortality of Asian citrus
2002. Influence of prey size on predation success by psyllid (Homoptera: Psyllidae) in central Florida.
Zelus longipes L. (Het., Reduviidae). J. Appl. Ento- Biol. Control: 29: 260-269.
mol. 126: 74-78. PEÑA, J. E., DUNCAN, R., AND JACAS, J. 2008. Dynam-
EDWARDS, J. S. 1966. Observations on the life history ics of mortality factors of the citrus psyllid in South
and predatory behaviour of Zelus exsanguis (Stål) Florida. Proc. Florida State Hort. Soc. 121: 113-117.
(Heteroptera: Reduviidae). Proc. R. Entomol. Soc. ROSENHEIM, J. A., WILHOIT, L. R., AND ARMER, C. A.
London (A): 21-24.41. 1993. Influence of intraguild predation among gen-
EVANS, H. F. 1976. Mutual interference between preda- eralist insect predators on the suppression of an her-
tory anthocorids. Ecol. Entomol. 1: 283-286. bivore population. Oecologia 96: 439-449.
HALL, D. G., HENTZ, M. G., AND ADAIR JR., R. C. 2008. SAS INSTITUTE. 2001. PROC user’s manual, version 6th
Population ecology and phenology of Diaphorina ed. SAS Institute, Cary, NC.
citri (Hemiptera: Psyllidae) in two Florida citrus VAN BAALEN, M., KRIVAN, V., VAN RIJN, P. C. J., AND
groves. Environ. Entomol. 37: 914-924. SABELIS, M. W. 2001. Alternative food, switching
HARIDASS, E., NOBLE MORRISON, M., AND BALU, A. predators, and the persistence of predator-prey sys-
1988. Predatory behaviour of Rhinocoris marginatus tems. American Nat. 157: 512-524.

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