Life history of Cybocephalus nipponicus Endrödy-Younga (Coleoptera: Cybocephalidae), a predator of Aulacaspis yasumatsui Takagi (Hemiptera: Diaspididae)

2006·6.9 MB·

by  Trevor Randall Smith

PROC. ENTOMOL. SOC. WASH.
108(4), 2006, pp. 905-916
LIFE HISTORY OF CYBOCEPHALUS NIPPONICUS ENDRODY-YOUNGA
(COLEOPTERA: CYBOCEPHALIDAE), A PREDATOR OF AULACASPIS
YASUMATSUI TAKAGI (HEMIPTERA: DIASPIDIDAE)
TREVOR RANDALL SMITH AND RONALD D. CAVE
(TRS) Department of Entomology and Nematology, University of Florida, P.O.
Box 110620, Gainesville, FL 32611, U.S.A. (e-mail: [email protected]); (RDC) Indian
River Research & Education Center, University of Florida, 2199 S Rock Road, Ft.
Pierce, FL 34945-3138, U.S.A. (e-mail: [email protected])
Abstract.4The life history of the predatory beetle Cyhbocephalus nipponicus
Endrody-Younga was studied by rearing the beetle on the cycad aulacaspis scale,
Aulacaspis yasumatsui Takagi. Mean development times of egg (7.3 + 0.8 days),
larval (13.7 + 1.1 days), and pupal (18.6 + 1.6 days) stages were determined.
Mortality in each life stage, adult longevity, and adult sex ratios also were measured.
A clarification of differences between C. nipponicus and C. binotatus is included.
Key Words: Beetles, biological control, life cycle, longevity, scale predator, cycads
Cybocephalids are one of the most each have very distinctive male genitalia
economically important groups of natu- (Endré6dy-Younga 1971) and C. binota-
ral enemies against scale insects (Alvarez tus (Fig. 1A) has two large black spots
and Van Driesche 1998a). Larvae and on the pronotum, which are absent in C.
adults are voracious predators and have nipponicus (Fig. 1B). Although C. nippo-
many desirable traits for use as biolog- nicus previously was established in Flor-
ical control agents. Cybocephalus nippo- ida before 1998 (according to specimen
nicus Endrédy-Y ounga was released and label data in the Florida State Collection
later established in the Washington D.C./ of Arthropods), its range and abundance
Maryland area to combat the euonymus in the state before 1998 is unknown
scale, Unaspis euonymi (Comstock) (Smith and Cave, in press).
(Drea and Carlson 1988, Drea and The cycad aulacaspis scale (CAS) is
Henrickson 1988). Alvarez and Van the most damaging scale found on
Driesche (1998a) later released and cycads in Florida (Hodges et al. 2003).
established populations of C. nipponicus CAS is native to Thailand but is found
in New England. This same species also throughout China and_ southeastern
was released, under the false identifica- Asia, as well as on several Caribbean
tion of Cybocephalus binotatus Grou- islands, Florida, and Hawai (Ben-Dov
velle, into the Miami area in 1998 for et al. 2003). In 1992, CAS had become
control of the cycad aulacaspis scale, such a problem in Hong Kong that 704
Aulacaspis yasumatsui Takagi (Anony- 100% mortality was recorded in infested
mous 1998, Howard et al. 1999, Howard king sagos, Cycas revoluta Thunberg
and Weissling 1999). While C. nipponicus (Hodgson and Martin 2001). The first
and C. binotatus appear similar, they detection of CAS in Florida occurred
906 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
in 1996 in Miami at the Montgomery CAS as prey, and compare these to the
Botanical Center. The scale was thought results from Tanaka and Inoue (1980)
to have arrived on infested cycads and Alvarez and Van Driesche (1998a)
imported from southeastern Asia (Ho- using euonymus scale as prey. A better
ward and Weissling 1999). By the end of understanding of these beetles using
1997, CAS had spread throughout M1- different prey will lead to greater un-
ami and as far north as Lake Okeecho- derstanding of how they perform as
bee and could be found on 20 species of biological control agents in the field,
cycads (Howard and Weissling 1999), and consequently increase success in
however it seems to prefer Cycas and controlling CAS.
Stangeria (Emshousen, personal commu-
MATERIALS AND METHODS
nication, 2004). This led to the spread
of CAS to Hawaii in 1998 through the A colony of CAS was reared on king
legal importation of infested cycads from sagos in a sealed greenhouse to keep out
Florida (Hodgson and Martin 2001). At possible predators and/or parasitoids.
present, CAS has been reported from Small king sagos were infested with
Pensacola east to Jacksonville and south CAS by placing large numbers (>100)
into the Florida Keys. Infested cycads in of eggs on each plant. Once infested,
northern Florida were suspected trans- plants were then placed in contact
plants from southern nurseries rather with other non-infested plants to spread
than natural progression of the scale non-parasitized scales to other plants.
northward. Thus, we could be confident that para-
The objective of this study is to collect sitoids and predators did not invade the
life history date on C. nipponicus using colony.
VOLUME 108, NUMBER 4 907
A colony of C. nipponicus was initiated CAS-infested leaflets on top of sterilized
from individuals collected in south Mi- sand: in) the <bottom of sthe> vial. Old
ami (25°38'21="N, 80°20'09"W). Aphanog- leaflets were replaced with fresh, infested
mus albicoxalis Evans and Dessart (Hy- leaflets every five days throughout the
menoptera: Ceraphronidae) parasitizes life cycle. A fine mesh cloth was placed
the pupae of C. nipponicus in southern over the top of the vials to allow airflow.
Florida (Evans et al. 2005), but this Larval and pupal development was
parasitoid was excluded by collecting checked daily. Upon emergence from
only adult beetles and subsequently rear- the pupal case the adults remained in
ing future generations in sealed cages plastic vials and were provided with 204
(ism < 0:5 .m X 0.5 m). Cycad leaves 30 fresh CAS every 3 days. Adults were
infested with CAS were cut from the checked daily until death.
colony plant, with rachis bases placed in Eggs, larvae, and pupae were critical-
floral water tubes for hydration, and point dried in a Tousimis®samdri-780 A,
then placed in rearing cages. The leaves and sputter coated with a gold-palladium
and interior of cage were misted with alloy. Images were taken with a JEOL®
distilled water every three days. A moist JSM-S5510LV scanning electron micro-
sponge also was provided for hydration. scope and a Syncroscopy® automontage
Leaves were replaced every three weeks. photography system.
Old leaves were held in separate cages for Descriptive statistics were generated in
three weeks to recover emerging beetles. SAS (2001) using a PROC UNIVARI-
Beetle and scale voucher specimens were ATE analysis. The dependent variable
placed in the Florida State Collection of was number of days in each stage and the
Arthropods (FSCA). independent variable was the stage itself.
All life cycle studies were carried out in PROC UNIVARIATE and PROC 1-test
temperature- and humidity-controlled were used to generate statistics for adult
cabinets set at 25°C with a relative longevity.
humidity of 80% and a photoperiod of
RESULTS AND DISCUSSION
14:10 (L:D). Each treatment was initiat-
ed by isolating 25-30 mating pairs of The egg of C. nipponicus is elongate
beetles randomly selected from the lab- oval with both ends rounded, relatively
oratory colony. Each pair was placed in large measuring 0.42 mm by 0.20 mm
a 25-dram plastic vial with one C. (n = 50) and usually light gray to purple.
revoluta leaflet infested with male and Eggs were usually found singly inside the
female CAS. After 24 hours the beetles vacated tubular cover of a male scale or
were removed and eggs collected from under the armor of a female scale,
beneath the scale armor on the leaflet. usually with a live scale beneath but
Eggs were measured (length and width), occasionally with a dead female. During
and then, to simulate natural conditions, low scale density, as many as 5 eggs
placed on the surface of a small, clean under one female armor were observed.
piece of C. revoluta leaflet and covered An egg deposited within the male scale
with the armor of an adult female CAS. cover fit snugly and had almost the same
The leaflet piece was placed in the well of diameter as the scale cover, thereby
a rectangular tissue culture dish, covered allowing only one egg to be placed in
with parafilm, and placed in the envi- one male cover. The surface was smooth
ronmental chamber. Eggs were checked aside from debris sticking to the surface
daily until larvae emerged. (Fig. 2) and was slightly tacky, allowing
Newly emerged larvae were placed in the egg to stick to the substrate. Females
25-dram plastic vials with freshly-cut, typically laid about 3 eggs per day and
908 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Cybhocephalus nipponicus. 2, Egg.u 3, First-instar larva dorsal habitus (A), ventral habitus (B).
&
VOLUME 108, NUMBER 4 909
Table 1. Development of Cybocephalus nipponicus on Aulacaspis yasumatsui.
SS
Stage Mean (Days) SE Range (min-max) (Days) N
Egg eS 0.1 4 (5-9) Sil
Larva [S57 0.1 4 (12-16) 94
Pupa 18.6 0.2 6 (16-22) 44
Total development time BOS
Male life-span 89.1 OFF. 146 (9-155) 23
Female life-span 110.0 9.6 175 (15-190) 3)
on average 288 eggs in a lifetime (Alvarez instars in Cybocephalus semiflavus Cham-
and Van Driesche 1998a). Eggs hatched pion. When molting, the cuticle ruptured
about 7 days after oviposition (Table 1). along the top of the head capsule and
Eyespots could be seen 142 days before along the median dorsal region of the
larval emergence. body. The larva emerged from _ the
When the larva emerged, the chorion anterior portion of the old exuviae first,
split along the longitudinal axis and the then wriggled vigorously to extract the
larva wriggled free. This process took posterior body portion. The posterior
about 15 minutes compared to the 30 to portion of the old exuviae remained
45 minutes reported by Blumberg and attached to the substrate. Average larval
Swirski (1982) on the life history of development was about 14 days (Ta-
Cybocephalus micans Reitter and Cybo- blew):
cephalus nigriceps nigriceps (J. Sahlbery). If bright light was shone on larvae
The neonate larvae were white or yel- they immediately moved underneath
lowish with long setae along the body, a scale armor or debris. Once disturbed
but after feeding for a day turned light larvae raised the head and body away
purple or lavender, with 4 black stem- from the leaf surface, arching the body
mata on each side of the head (Figs. 3A, into a C-shape, and holding to the
B). Not only were larvae covered in long, substrate with the conical protuberance
slender setae but also shorter trumpet- found on segments 8 and 9. This threat
shaped setae (Fig. 4). After emergence, posture is similar to that used by the
larvae immediately began to feed either larvae to extract themselves from old
on the scale eggs sharing the space exuviae.
beneath the armor or rarely on the Larvae became less active 2 to 3 days
female scale. If an egg hatched in a male prior to pupation, stopped feeding, and
scale cover, the larva would go to the eventually becoming immobile and at-
nearest food source. Larvae continued to taching the posterior of the abdomen to
move from scale to scale feeding on the substrate before forming the pupal
males, females, and eggs but spent the case. Larvae gathered pieces of scale
most time underneath female armor. armor and incorporated these pieces into
They also were seen cannibalizing other an ovoid pupal chamber with one end
larvae when scale density was extremely flatter where it attached to the substrate
low, as mentioned by Alvarez and Van (Fig. 6A).
Driesche (1998a). Larvae fed for 9 to Pupal chambers often were found in
10 days. the anterior portion between leaflet and
Three instars (Figs. 5A, B) were ob- leaf rachis or near the leaflet base.
served, similar to C. micans and C. n. However, pupal chambers also were
nigriceps (Blumberg and Swirski 1982). observed along leaflet and rachis. When
However, Ahmad (1970) recorded four not given access to scales, larvae used
PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Fig. 4. Short trumpet-shaped setae on third-instar larva of Cybocephalus nipponicus.
sand or other organic material to con- tions could be produced per year in
struct the pupal chamber (Fig. 6B), southern Florida or other areas with
sometimes attaching to the leaf or amenable temperatures. Alvarez and
dropping to the sand. Infrequently, Van Driesche (1998a) suggested that
larvae dropped to the sand and made these beetles were capable of producing
a sand cocoon even when scales were 3 generations per year in New England.
available. This behavior is common in Preoviposition lasted about 4 days (n
Cybhocephalus and has been suggested or = 29) with some females laying eggs as
recorded for other species (Clausen and early as 2 days (n = 2) after emergence.
Berry 1932, Flanders 1934, Smirnoff Adults (Fig. 8) began feeding soon after
1954, Blumberg and Swirski 1982). All emergence and consumed an average of 4
pupae exhibited typical exarate features scales per day, with females typically
(Figs. 7A, B). Pupation lasted about eating more than the males. Dispropor-
18 days (Table 1). Beetles exited the tionate feeding is probably due to size,
chamber by chewing an emergence hole. because males are smaller than the
There was no significant difference in females. Maximum female longevity
development time from egg to adult was 190 days, with an average of about
between sexes (¢ = 1.50, df = 52, P = 110 days (Table 1). Average longevity
0.1389). Total development from egg to of males was 89 days (Table 1) with
adult lasted about 40 days (Table 1), a maximum of 155 days. Due to high
thus it is conceivable that 748 genera- variation, a f-test showed no significant
VOLUME 108, NUMBER 4
S68 sm
Figs. 5-6. Cybocephalus nipponicus. 5, Third-instar larva dorsal habitus (A), ventral oblique habitus
(B). 6, Pupal chamber made from female scale covers (A), chamber made from sand (B).
912 PROCEEDINGS OF THE ENTOMOLOG NGTON
/ , . ya's ne die 5
Figs. 7-8. Cybhocephalus nipponicus. 7, Pupa dorsal habitus (A), ventral habitus (B). 8), Adult, lateral habitus.
VOLUME 108, NUMBER 4 S18
Table 2. Mortality (%) of immature stages of rates in our study also were slightly
Cybocephalus nipponicus reared on Aulacaspis higher, possibly due to high humidity.
yvasumatsui (n=200). Fungal growth was a consistent problem
in the humid environment of our rearing
No. Alive at No. Dying in Apparent
Stage (x) Start (1x) Stage (d,) Mortality (qx) chambers. Scales often became so en-
Egg 200 44 0.22 crusted on the cycad leaflet that sapro-
Larva 156 134 0.86 phytic fungi quickly spread. Alvarez and
Pupa 2p D, 0.09 Van Driesche (1998a) did not record
Adult 20 relative humidity, thus a comparison
cannot be made.
Mortality was highest during the
difference between longevity of the sexes
larval stage. The first few days of larval
(¢ = 1.50, df = 52, P = 0.1389). These
development proved to be most difficult
findings are intermediate between the
(Fig. 9). Eggs and pupae seemed to be
78 days for males and 99 days for
quite hardy with mortality of 22% and
females reported by Alvarez and Van
9%, respectively (Table 2), which are
Driesche (1998a) at 22°C and 122 days
similar to the 14% and 8% mortality
for males and 143 days for females
rates found by Alvarez and Van Driesche
reported by Tanaka and Inoue (1980),
(1998a). Therefore, the 86% mortality
who do not detail their experimental
rate in the larval stage (Table 2) is
temperatures used. Shorter male longev-
interesting and not predicted. However,
ity may be due to their more active
when reared on San Jose scale, Quad-
nature. Males were observed moving
raspidiotus perniciosus (Comstock), Al-
around the cages more often than varez and Van Driesche (1998a) found
females. Often, 5 or 6 males would chase the larval stage of C. nipponicus had
a female for hours before finding a new a correspondingly high 77% mortality
female to; jpursue. The Sex ratio of rate.
emerging adults was 23:31 (male:female). Certain aspects of the biology and life
Our results were similar to those of history of other Cybocephalus species
Alvarez and Van Driesche (1998a) and have been studied, typically as part of
Tanaka and Inoue (1980). However, all biological control projects, e.g., Cyboceph-
stages developed slower in the former alus rufifrons Reitter (DeMarzo 1995),
study (9.1 days for eggs, 14.5 days for Cybhocephalus freyi Endrody-Younga
larvae, and 20.4 days for pupae) in (Lupi 2003), and Cyhbocephalus fordori
comparison to our results, but this may Endrédy-Younga (Katsoyannos 1984)
be due to their lower experimental have been studied in Europe; and Cybo-
temperatures or the food source. Popu- cephalus. semiflavus Champion (Ahmad
lation differences may account for some 1970) and Cybhocephalus gibbulus Erichson
discrepancies in the life history parame- (Nohara and Iwata 1988) have been
ters of the beetles in each study. The studied in Asia. In the Middle East,
beetles studied by Tanaka and Inoue several studies have been carried out on
(1980) originated in Japan and those C. aegyptiacus, C. binotatus, C. micans,
studied by Alvarez and Van Driesche and C. n. nigriceps (Blumberg 1973, 1976;
(1998a) originated in Beijing, China. Our Blumberg and Swirski 1974 a, b, 1982). In
beetles may have originated in Thailand, Australia, Kirejtshuk et al. (1997) de-
however, this is only speculation consid- scribed Cybocephalus aleyrodephagus and
ering the beetles were present in Florida studied its life cycle. The life histories of
before the recorded introduction in 1998 these species do not differ dramatically
(Smith and Cave, in press). Mortality from C. nipponicus, and there seems to be
914 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
a
%Mo rtality
a] T Ue T T T 1
8-9 10 Wy 12) tS 4a
Age in Days
Fig. 9: Larval mortality of Cybocephalus nipponicus over time.
fairly consistent life cycle and feeding that provide a larger food source and
habits. require less searching (Alvarez and Van
In the absence of prey, female cyboceph- Driesche 1998b). Alvarez and Van
alids are able to withhold eggs for up Driesche (1998b) found that the highest
to 2 days, indicating that oviposition larval survival rate could be found in
strategy is not only governed by food larvae feeding on scales older than
consumption but also by qualitative 30 days. Blumberg and Swirski (1982)
features of the scale population (Alvarez noted that C. n. nigriceps rarely laid eggs
and Van Driesche 1998b). In the pres- under dead female scales.
ence of high scale density, cybocephalids Evans et al. (2005) described two
increase egg production until an asymp- species of Aphanogmus (Ceraphronidae)
tote is reached. Again, this allows that parasitize C. nipponicus pupae.
cybocephalids to maintain their popula- Aphanogmus inamicus Evans and Dessart
tions at low scale densities. If circum- emerged in quarantine from hosts col-
stances allow, female cybocephalids will lected in Thailand, and A. albicoxalis
lay only one egg under a single scale occurs naturally in Florida. The latter
cover. However, if the number of scales species is broadly distributed in southern
in a patch is low, and the beetle cannot Florida, with collection sites in Collier,
find new scales, it will lay eggs under Miami-Dade, and St. Lucie counties.
a scale under which eggs are already The levels of parasitism in C. nipponicus
present (Alvarez and Van _ Driesche populations in Florida are currently
1998b). The beetle larvae are forced to undetermined, but large numbers of
consume more prey when feeding on these wasps occasionally have been seen
younger scales, therefore for greater on cycads.
offspring survivability female cyboceph- Cyhocephalus nipponicus probably al-
alids prefer oviposition on older scales ways will be considered a supplementary