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BioControlJournal of the InternationalOrganization for Biological Control ISSN 1386-6141 BioControlDOI 10.1007/s10526-014-9619-2

Field study demonstrates that exoticparasitoids (Hymenoptera: Encyrtidae) ofmealybugs (Hemiptera: Pseudococcidae)are absent from a native forest habitat inNew ZealandJohn G. Charles, Shaun A. Forgie, AshaChhagan & Robert D. Edwards

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Field study demonstrates that exotic parasitoids(Hymenoptera: Encyrtidae) of mealybugs (Hemiptera:Pseudococcidae) are absent from a native forest habitatin New Zealand

John G. Charles • Shaun A. Forgie •

Asha Chhagan • Robert D. Edwards

Received: 18 March 2014 / Accepted: 5 September 2014

� International Organization for Biological Control (IOBC) 2014

Abstract Laboratory-based, physiological host-range

tests of classical biocontrol agents may be complemented

by examining the ecological (realised) host-range of

similar, previously established species. Sentinel long-

tailed mealybugs (Pseudococcus longispinus (Targioni-

Tozzetti)) on potted citrus plants, and two species of

native mealybugs on potted native trees, were placed in

pairs in an orchard and a native forest block 500 m away.

Sentinel P. longispinus on citrus plants were also placed

along transects anchored in each habitat and extending

towards the other by 100–150 m. Parasitoids were reared

from the retrieved mealybugs. P. longispinus in the

orchard was regularly parasitized by four species of

exotic Encyrtidae, but was never parasitized by them in

the native forest even though the parasitoids were present

in the surrounding environment. Sentinel native

mealybugs were not parasitized by any species in either

habitat, although native parasitoids (especially Errolium

sp. (Hym: Platygastridae) and unidentified Hym: Aphe-

linidae) were collected from native mealybugs within the

native forest.

Keywords Long-tailed mealybug � Pseudococcus

longispinus � Exotic parasitoids � Native parasitoids �Risk assessment

Introduction

A key component of modern classical biological

control programmes against insect pests is an assess-

ment of the threat that the proposed new natural enemy

poses to non-target fauna—especially native and

economically valued species. The threat is usually

estimated through host-specificity tests, carried out in

a containment laboratory by exposing selected species

to the biocontrol agent (usually a parasitoid). Both the

selection of host species to test and the test method-

ologies for different natural enemies have been placed

on an increasingly scientific footing in recent years

(e.g. Kuhlmann et al. 2006). Yet, almost inevitably,

the artificial constraints of containment laboratories

mean that many of the ecological inputs that limit the

host range of natural enemies in nature are absent. As a

result, laboratory ‘no-choice’ or even ‘choice’ exper-

iments may provide accurate measures of a biocontrol

agent’s physiological host range, but overestimate its

Handling Editor: Dirk Babendreier.

J. G. Charles (&) � S. A. Forgie � A. Chhagan �R. D. Edwards

The New Zealand Institute for Plant & Food Research

Limited, Mt Albert, Private Bag 92169, Auckland 1142,

New Zealand

e-mail: john.charles@plantandfood.co.nz

J. G. Charles � S. A. Forgie � A. Chhagan � R. D. Edwards

Better Border Biosecurity NZ, Auckland, New Zealand

Present Address:

S. A. Forgie

Landcare Research, Private Bag 92170, Auckland 1142,

New Zealand

123

BioControl

DOI 10.1007/s10526-014-9619-2

Author's personal copy

real or ecological host range. Even if the constraints of

containment could be overcome, it is rarely feasible to

test all the native species that the proposed biocontrol

agent will encounter in its new environment.

One way to improve measures of a natural enemy’s

ecological host range is to conduct extensive field

collections in the country(ies) in which it is naturally

found (e.g. Barratt et al. 2012). An obvious limitation

of this approach is that it cannot test for the enemy’s

potential host range among the new fauna to which it

will be exposed in its proposed destination. Additional

information can be obtained from the destination

country by examining the host range of exotic natural

enemies that are closely related to the proposed new

biocontrol agent, and which have already established

either through deliberate or accidental introduction

(Charles and Allan 2002). The extent to which these

species have (or have not) formed new ecological

associations can be used to predict the potential threat

posed by the proposed new enemy, and has increasing

value with the elapsed time since establishment.

This approach may be particularly valuable for

studying parasitoids that typically co-evolve close

relationships with their hosts, such as those Encyrtidae

(Hymenoptera) that are effective natural enemies of

mealybugs (Hemiptera: Pseudococcidae) (Moore

1988), and are often monophagous or narrowly oli-

gophagous at the host species level (Charles 2011). The

long-tailed mealybug, Pseudococcus longispinus (Tar-

gioni-Tozzetti), is native to the eastern seaboard of

Australia, but has been a pest in New Zealand for more

than 100 years (Charles 1998a). No parasitoids have

been deliberately introduced, although the predatory

Cryptolaemus montrouzieri Mulsant (Coleoptera: Coc-

cinellidae) was imported in a classical biocontrol

programme in the late 1890s (Charles 1989). Yet P.

longispinus is commonly attacked by several species of

effectively host specific Encyrtidae, also probably of

Australian origin, which have self-established naturally

over many years (Charles 1993; Charles et al. 2010). No

exotic encyrtid has ever been reared from New

Zealand’s endemic mealybugs which are, however,

attacked by native parasitoids (Noyes 1988; Charles and

Allan 2002). However, little is known of the biology of

the more than 115 species (Cox 1987) of native

mealybugs, or of their natural enemy fauna, so, from a

risk assessment perspective, the absence of parasitism

by exotic parasitoids could be considered a function of

insufficient collection data.

To investigate this conundrum, we report on

sentinel experiments using P. longispinus and native

mealybugs in both a mature citrus orchard and a

nearby patch of remnant native forest. We aimed to

determine the extent to which exotic and native

parasitoids were present in these neighbouring habitats

and to test the hypothesis that native mealybugs in

native habitats are not threatened by immigration

pressure from well-established, exotic parasitoids of

exotic mealybugs in modified habitats.

Methods

Habitats

Mealybugs and their parasitoids were collected from

two nearby habitats within a rural setting north-west of

Auckland city, New Zealand (36�4401800S,

174�2602700E) and 8 m asl. One habitat was a small

(c. 2 ha) citrus orchard (hereafter called the ‘orchard’)

with blocks of c. 15-year-old lemons and grapefruit

(unknown cultivars), and mainly exotic species of

ornamentals in the gardens surrounding the orchard

homestead. No insecticides were applied to the

orchard either immediately prior to, or during the

experiments. The other habitat was a privately owned

5-ha isolated, remnant stand of native forest (hereafter

called the ‘bush’) located 0.5 km due south of the

orchard. The bush was characterised by a tree canopy

noticeably of large Agathis australis ((D. Don)

Loudon and Dacrycarpus dacrydioides ((A. Richard)

de Laubenfels). The block had not been logged for

many years (if at all), and was fenced to keep out

livestock. The absence of mammalian grazing allowed

the establishment of a diverse understorey of indige-

nous trees and shrubs. Common species included

Dysoxylum spectabile ((Forst. f.) Hook. f.), Hedycarya

arborea (J. R. Forst. & G. Forst.), Melicytus ramiflorus

(J. R. Forst. & G. Forst.), Macropiper excelsum Miq.

and Myrsine australis (A. Rich.) Allan, all of which

are known hosts for native mealybug species (Cox

1987) and which could be conveniently sampled by

hand from the ground. The area in between the two

sites consisted of private properties, mostly in pasture

grazed by livestock and interspersed with a few

buildings, farm access tracks and isolated exotic tree

species which had been planted mainly for shade for

stock and amenity/privacy. The trees were not

J. G. Charles et al.

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identified, nor were any sampled for the presence of

mealybugs. The overall habitat was typical of the

rural, modified landscapes found immediately north of

Auckland, with the exception of the unusual presence

of the remnant bush block.

Mealybug and parasitoid collections

Naturally occurring mealybugs and natural enemies in

the orchard and bush were collected through visual

searches. Typically, native mealybugs were patchily

distributed and often uncommon and if mealybugs

themselves escaped detection by human searchers,

then so did any associated parasitoids. Hence a second

technique used sentinel mealybugs to determine

whether exotic parasitoids were present in the bush,

or native parasitoids in the orchard. The two tech-

niques are described further below.

Visual searches

The natural occurrence of mealybugs and their natural

enemies in both the orchard and bush were examined

by visual searches in citrus trees or understorey trees

and shrubs respectively. Between 10 % and 50 % of

mealybugs collected from orchards in summer are

typically parasitized (Charles 1998b; Charles et al.

2010, Charles unpublished), so a search time that

delivered from 30 to 100 mealybugs was considered

adequate to locate the presence or absence of parasit-

oids. This number of mealybugs was usually collected

in 40–60 min searches in both orchard and bush

habitats. Each search was conducted in approximately

the same area of habitat on each occasion, examining

shoots and foliage up to c. 2 m above ground level.

Mealybugs (P. longispinus) in the citrus orchard were

identified by sight. In the bush, plant species known to

be hosts of mealybugs were examined as they were

encountered, and any mealybug infested leaves or

shoots were removed into a paper bag.

In the laboratory, mealybug predators were

removed and identified. Neonate P. longispinus

(which are not parasitized during the several days

they remain with their mother before dispersing) were

also removed. A sample of adult, ovipositing mealy-

bugs from the bush were photographed in Situ, and

then removed to alcohol for slide mounting and

identification under a microscope. The remaining

mealybugs from both sites were held for 3–4 weeks

either on pesticide-free potatoes (P. longispinus) or on

host plant foliage (native mealybugs) to allow internal

parasitoids to complete development and to mummify

their mealybug hosts. All life-stages of the native

mealybugs were retained for development because it

was unknown if first instars may have been parasit-

ized. Mummies were then transferred individually to

gelatine capsules to await emergence and identifica-

tion. Searches for mealybugs were made on four

occasions (December 2006, April 2008, January 2009

and December 2009), to coincide with experiments

when sentinel mealybugs were placed within the

orchard and bush.

Sentinel mealybugs on potted plants

Experiments to trap parasitoids in the orchard and

bush were conducted using sentinel mealybugs feed-

ing on whole potted plants that were placed experi-

mentally in different habitats for short time periods.

Sentinel mealybugs have been used previously to

record parasitism (Charles et al. 2004). On that

occasion, obscure mealybug (Pseudococcus viburni

(Signoret)) feeding on potatoes were tied on to apple

trees and successfully recorded the establishment of

the newly released parasitoid Acerophagus maculi-

pennis. However, sentinel native mealybugs do not

successfully establish and feed on potatoes, so in the

current experiment they could only be deployed on

native host plants. Although P. longispinus do feed on

potatoes, they were also deployed on citrus host plants

of similar size and form to the native plants, to allow

comparison and to provide a more natural environ-

ment for host-seeking parasitoids. The host location

behaviours of native parasitoids of mealybugs or those

of P. longispinus are essentially unknown, but are

presumed to rely on a combination of long and short

range volatile and contact chemical cues. It was hence

presumed that the mealybug parasitoids sought in this

experiment: (a) were attracted to hosts and did not

search randomly, and (b) responded both rapidly and

accurately to received cues. The role that host density

plays in the searching efficiency of these parasitoids is

also unknown, but they naturally locate mealybug

hosts that are typically patchily distributed within their

host plant and habitat. Such a distribution was

impossible to replicate with these experiments, but it

was also presumed that sentinel mealybugs on the

experimental potted plants would provide a relatively

Field study demonstrates that exotic parasitoids of mealybugs

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large host patch compared with the surrounding

habitat, and that they would be rapidly and efficiently

located by searching female parasitoids.

The first experiment was conducted in summer

(from December 2006 to January 2007) to compare the

natural enemy attack on exotic and native mealybugs

placed artificially both in the orchard and the bush.

About three months prior to deployment, potted host

plants grown in plastic planter bags within a shade-

house were trimmed to a height of c. 1.2 m. They were

infested with mealybugs by placing 20–30 mature

adult females on to the foliage and allowing them to

disperse and settle at will through the plant. The exotic

mealybug (P. longispinus) was established on ‘Yen

Ben’ lemon plants. The native Paracoccus glaucus

(Maskell) and Paracoccus zealandicus (Ezzat &

McConnell) were established on potted Hedycarya

arborea plants. Over a period of 6–8 weeks, the

female mealybugs produced crawlers which dispersed

freely and then settled to feed. Once mealybugs of

different ages were apparent, the plants were trans-

ferred to the field sites. Before taking the plants into

the field, the roots were soaked to saturation in water,

and each pot was then placed in a plastic bag, loosely

tied around the trunk of the tree, to keep the roots moist

during the experiment.

A citrus and a native plant were allocated in

matched pairs to five locations each within the orchard

and the bush. In the orchard, each member of a pair

was placed on the ground on either side of the trunk of

three different mature lemon trees. The upper half to

one third of these sentinel plants extended into the

lemon tree canopy. The two remaining pairs were

placed within the canopies of two grapefruit trees,

about twice the size of the lemon trees and growing in

the homestead gardens about 30–50 m from the

sentinel mealybugs in the orchard trees. In the bush,

the sentinel plant pairs were placed on the ground, next

to one or more of the native understorey trees or shrubs

(identified above) that were known hosts of P. glaucus

and P. zealandicus, and with their foliage interspersed

as much as possible. The spatial distribution of the

sentinel plants in the bush depended on the locations of

suitable native plants, but was of a similar scale to

those in the orchard with each pair about 10–20 m

apart within an area of about 50 m diameter.

Native mealybugs did not establish on the native

plants, and collecting and maintaining seasonal pop-

ulations of sentinel mealybugs each year proved to be

impractically time-consuming. Hence two subsequent

experiments were carried out in April 2008 and

January 2009 with sentinel P. longispinus on citrus

plants only. In April 2008, five potted plants were

placed in the orchard and five in the bush, at the same

locations as in the first trial. In January 2009, an

additional P. longispinus-infested citrus plant was

placed in the orchard and the bush, i.e. six plants per

site.

The day before the potted plants for each trial were

placed in the field, the numbers of mealybugs on each

of ten uniquely identified and tagged mealybug

infested leaves on each plant were counted. The plants

were retrieved after 14, 19, and 14 days for each of the

three experiments respectively. The additional five

days in April 2008 was allowed because it was

suspected that cold and wet weather for much of the

first 14 days may have restricted the flight and

searching activities of natural enemies.

When retrieved from the field sites, each plant was

immediately enclosed in a plastic bag to minimise the

escape of any mobile natural enemies during transit to

the laboratory, where each plant was examined within

24 h. Any predators were removed and identified. The

numbers of mealybugs on the tagged leaves were

counted again. The remaining leaves were examined

for mealybug presence, and the mealybugs on the first

ten infested leaves were also collected. The mealybugs

from all 20 leaves were then reared for about 21 days

to allow internal parasitoids to develop. Leaves with P.

longispinus were placed in plastic containers with

sprouting potatoes, on to which the mealybugs were

free to crawl. The native mealybugs from experiment

1 were held on their host leaves in 9-cm Petri dishes

with slots cut in the rim through which the leaf stalks

protruded into a vial of fresh water.

Mealybugs were examined every 2–3 days and all

mummies were removed to individual gelatine cap-

sules for parasitoid emergence. The numbers of

mummies retrieved and the species/sex of parasitoids

that emerged were recorded from each site and

occasion.

Temperatures in the orchard and bush were mea-

sured in April 2008, to compare an abiotic factor that

might limit host searching by parasitoids. A data

logger (Tinytag Talk) was tied to a tree branch (c.

1.5 m above ground level) in each of the orchard and

bush for the 19 days of the trial, and set to record

temperatures every 2 h. The data loggers were

J. G. Charles et al.

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interrogated to deliver maximum, minimum and mean

temperatures.

To provide an estimate of mealybug dispersal from

tagged leaves within a plant when undisturbed, a

control plant was held in a predator-free shade house

during the course of the April 2008 experiment.

Mealybug numbers on ten tagged leaves were

recorded on the same days that the sentinel mealybugs

were deployed and retrieved from the field.

Sentinel mealybugs to detect exotic parasitoids

outside the orchard

If native mealybugs in the bush were indeed

threatened by immigration from exotic parasitoids in

the orchard, then those parasitoids must disperse

between the two habitats. Individual small hymenop-

teran parasitoids (such as Mymaridae and presumably

Encyrtidae) are known to search over long distances

(in the order of kilometres) while locating hosts, so it

was presumed that the mealybug parasitoids were able

to actively disperse between the habitats (i.e. that the c.

500 m separation between the two habitats did not

form a spatial barrier between them). Such dispersal

may be continuous, seasonal (e.g. for a short period

every year induced by declining host numbers or intra-

specific competition), or be a rare event, dependent,

perhaps, on abiotic events (e.g. strong winds). To

provide an insight into the level of emigration from the

orchard, sentinel P. longispinus on citrus plants were

placed at increasing distances away from the orchard

(Fig. 1). Five potted citrus trees were infested by P.

longispinus as above, and placed about 30 m apart in a

more or less linear transect about 100 m long anchored

in the orchard (the ‘orchard transect’) and extending

towards the bush. Each potted plant was placed within

the canopy of, or next to, an existing tree (as described

above). To investigate immigration pressure on the

bush, a similar transect was anchored in the bush (the

‘bush transect’) and extended towards the orchard. For

the orchard transect, two potted plants were placed in

citrus trees 30–50 m from the orchard boundary and

three were placed in shelter trees up to 75 m beyond

the orchard in the direction of the bush. The bush

transect was similar in design, with the three potted

plants beyond the boundary extending about 75 m

towards the orchard. The trees into which the sentinel

mealybugs were placed outside the orchard and bush

provided shelter and shade for stock within an

essentially two-dimensional pasture habitat. The tree

species included exotic willows (Salix sp.), which are

known to host P. longispinus, but they were not

examined for the presence of existing mealybug

populations. The experiment was conducted in

December 2009 (Transect 1), and repeated in April

2010 (Transect 2) when six potted citrus trees were

used in each of the orchard and bush transect. For

Transect 2, two potted trees were placed in the orchard

or bush, one on the boundary, and three beyond the

boundary (Fig. 1). The potted citrus trees from both

experiments were retrieved after 14 days. The num-

bers of mealybugs on ten tagged, infested leaves per

plant were counted prior to deployment and again on

retrieval.

Statistical methods

The experiments were essentially qualitative in nature,

relying on the presence of host mealybugs as ‘bait’ to

attract and catch parasitoids for identification. The

numbers of mealybugs on selected leaves of each plant

were counted before deployment to ensure that there

were sufficient sentinel mealybugs on the plants, and

that the densities (of P. longispinus and native mealy-

bugs) on each plant were initially similar, but the

experiments were not designed to quantify changes or

losses in numbers of mealybugs. As long as there were

sufficient mealybugs to attract parasitoids during the

experiment their ultimate fate was of little interest.

However, it soon became apparent that the numbers of

sentinel mealybugs on most of the potted plants did

decline during the deployment period, and so the

numbers of mealybugs on the tagged leaves of each

plant when retrieved from the field were also counted.

The null hypothesis Ho that there was no change in the

number of mealybugs per leaf was tested by performing

a paired t test on log (count ?1) numbers of mealybugs

on each tagged leaf before and after deployment.

Results

Mealybug and parasitoid collections

Naturally occurring mealybugs

Pseudococcus longispinus was the only mealybug

species found naturally in the orchard, apart from a

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single, unparasitised, adult female P. viburni (plus

ovisac). All life-stages were commonly found on each

sampling occasion, when from 30 to 80 individuals

older than first instar were held for parasitoid rearing.

Four species of native mealybugs were regularly

collected on sub-canopy trees and shrubs in the bush.

Paracoccus zealandicus was collected from leaves of

Dysoxylum spectabile ((G. Forst) Hook. f.), Hedy-

carya arborea (J. R. Forst. & G. Forst.) and Melicytus

ramiflorus (J. R. Forst. & G. Forst.); Paracoccus

glaucus was collected from Macropiper excelsum

Miq. and Myrsine australis (A. Rich.) Allan; Dysmi-

coccus ambiguus (Morrison) was collected from

Dysoxylum spectabile, Macropiper excelsum and

Myrsine australis; and Rastrococcus namartini Wil-

liams & Henderson was collected from Myrsine

australis. All species were most frequently found in

November and December, but numbers collected per

occasion were usually lower (c. 20–50 s instar and

older) than those of P. longispinus in the orchard.

Naturally occurring predators and parasitoids of

P. longispinus in the orchard

Several species of generalist, mostly exotic predators,

including spiders (Araneae), ladybirds (Coleoptera;

Coccinellidae) and lacewings (Neuroptera: Coniopte-

rigidae and Hemerobiidae), which are known to prey

on mealybugs, were collected. Most predators were

found in association with high numbers of citrus

whitefly (Orchamoplatus citri (Takahashi) (Hemip-

tera: Aleyrodidae)), a new pest of citrus since 2000

(Gill 2001), with no known parasitoids in New

Zealand. Fifty-seven (29 %) of the 198 naturally

occurring P. longispinus collected from the orchard

over the four sample periods became mummified, and

four species of exotic parasitoids (all encyrtids) were

reared from them, most commonly from mid- to late-

summer. The species were Tetracnemoidea sydney-

ensis (Timberlake), Anagyrus fusciventris (Girault),

Gyranusoidea advena Beardsley and Parectromoides

varipes (Girault) (Table 1).

Naturally occurring predators and parasitoids

of native mealybugs in the bush

The only associated predators were midges (Diptera:

Cecidomyiidae), which were reared from larvae found

eating unidentified mealybugs on two occasions. The

adult midges were similar in appearance to Diadiplo-

sis koebelei (Koebele) (Charles 1985), but could not be

identified to species. A total of approximately 150

1 2 3 4 5 6 6 5 4 3 2 1

1

6

= Transect start

= Transect end

Orchard Bush

350 metres

75 metres

N S

WE

Fig. 1 Schematic representation of the relative location of sentinel mealybugs on potted citrus plants deployed between the orchard

and bush habitats in December 2009 and April 2010

J. G. Charles et al.

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native mealybugs older than 2nd instar were collected

during the four timed searches lasting for 150 min.

Only six (4 %) became mummified, but an additional

five mummies were collected with exit holes from

which unknown parasitoids had emerged. Two of the

six mummies from which parasitoids emerged in the

laboratory held Errolium sp. (Hymenoptera: Platygas-

tridae) (Masner and Huggert 1989), and four held

Coccophagus sp. (Hymenoptera: Aphelinidae). Spec-

imens of the undescribed species of Errolium were

reared from cocooned male mealybugs. Twin Erroli-

um embryos developed in each mealybug. They

matured at the same time, one emerging as a female

and the other as a male which had developed within a

distinctive pouch on the side of the mummy. The male

presumably mated with the female on (or prior to)

emergence and died soon after. The dark brown alate

female was much larger than the pale brown male,

which was tiny (\0.2 mm long), apterous and blind,

and was often difficult to locate within the gelatine

capsule, even with the aid of a binocular microscope.

Sentinel mealybugs and their natural enemies

on potted plants

The numbers of P. longispinus on the tagged leaves of

the control plant in the predator-free shadehouse did

not change significantly over 14 days (initial mean

number per leaf ± SE = 16.1 ± 3.0, final mean

number per leaf = 18.5 ± 2.9: paired t test;

P = 0.08, t = 1.97, df = 9). This indicated that

undisturbed, feeding mealybugs were quite sedentary

over a period of a couple of weeks, and is consistent

with preliminary (unpublished) observations that the

mealybugs did not often move from established

feeding sites in the absence of major biotic or abiotic

disturbance. During the 14 days of the late December

2006 experiment, temperatures in both experimental

habitats were similar, with the data loggers recording

means of 14.3 �C (range 5.4–21.6 �C) and 14.6 �C

(range 7.8–22.4 �C) in the orchard and bush respec-

tively. Given these data, it was expected that the

numbers of sentinel mealybugs retrieved at the end of

the experiments would not be different from those at

the beginning. However, numbers of all species of

sentinel mealybugs (Pseudococcus longispinus and

Paracoccus spp.) on tagged leaves of plants placed in

the orchard declined significantly during the deploy-

ment period (Table 2). In the bush, the numbers of P.

longispinus on the tagged citrus leaves did not change

during the experiment (although numbers were lower

than those on the tagged leaves in the orchard plants),

while the numbers of both Paracoccus species in the

bush declined to the same extent as did those in the

orchard (Table 2). Numbers of sentinel P. longispinus

per tagged leaf on the potted citrus trees deployed in

April 2008 also declined (Table 2). The initial num-

bers of sentinel P. longispinus per potted citrus-tree

leaf were lower in January 2009 than for the previous

two deployments, and there was again a very signif-

icant reduction after 14 days in both the orchard and

bush (Table 2). Despite the reduction in host numbers,

parasitoids were reared from P. longispinus on all

occasions that they were deployed in the orchard

(Table 3). The parasitoids were the same species

collected during the visual searches for naturally

occurring mealybugs, and similar percentages

(11–52 %) of parasitized mealybugs were collected

(Table 3). A few generalist predators (adults and

larvae of Orcus chalybeus (Boisduval) (Coleoptera:

Coccinellidae) and larvae of Melanostoma fasciatum

(Macquart) (Diptera: Syrphidae)) were also found

feeding on the sentinel P. longispinus, reflecting the

high numbers occurring naturally in the orchard. By

Table 1 Naturally occurring parasitoids (all Hym.: Encyrtidae) reared from Pseudococcus longispinus (second instar and older)

collected from orchard trees during visual searches

Date Number of P. longispinus

collected

Number of mummies

(% P. longispinus collected)

Numbers of each parasitoid species reared from mummies*

Tsyd Pvar Gadv Afusc

18/4/08 40 12 (30) 5 2 5 0

6/5/08 49 21 (43) 5 7 8 0

13/1/09 79 18 (23) 2 9 1 5

9/12/09 30 6 (20) 0 6 0 0

Tsyd Tetracnemoidea sydneyensis; Pvar Parectromoides varipes; Gadv Gyranusoidea advena; Afusc Anagyrus fusciventris

* parasitoids failed to emerge from two of the mummies

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contrast, none of the [1,000 sentinel P. longispinus

retrieved from the citrus plants placed in the bush was

parasitized—either by exotic or by native parasitoids

(Table 3).

More than 50 individual sentinel mealybugs of both

native species (Paracoccus glaucus and Paracoccus

zealandicus) were recovered from potted trees on 4

January 2007. However, no predator or parasitoid,

either native or exotic, was collected or reared from

any native mealybug retrieved from any sentinel tree.

Sentinel mealybugs to detect exotic parasitoids

outside the orchard

The initial numbers of sentinel P. longispinus per

tagged leaf on the potted plants deployed in the

orchard and bush transects in December 2009 and

April 2010 were similar, (Dec 2009: P = 0.06,

t = 1.91, df = 98; April 2010: P = 0.22, t = 1.22,

df = 118) (Table 4). However, after 14 days the

mealybug numbers had declined significantly in both

experiments. In 2009 (Transect 1), there were signif-

icantly fewer mealybugs remaining on the leaves from

the orchard transect than from the bush transect

(P = 0.002, t = 3.16, df = 98), but in 2010 (Transect

2) there were significantly fewer mealybugs remaining

on the leaves from the bush transect than the orchard

transect (P = 0.002, t = 3.16, df = 118) (Table 4).

On some trees no mealybugs remained, with no

evidence of their fate.

Three species of exotic parasitoids (P. varipes, T.

sydneyensis, and A. fusciventris) were reared from

Table 2 Mean number of sentinel mealybugs per tagged leaf (±SE) (untransformed numbers per leaf) on potted trees at start and end of

experimental periods, and test statistics for the null hypothesis of no change per leaf (paired t test on log (count ?1) mealybugs per leaf)

Species and date Orchard Bush

No. at start No. at end Test statistics No. at start No. at end Test statistics

Paracoccus glaucus

20/12/06–4/1/07 2.6 ± 0.52 1.5 ± 0.37 P \ 0.05

t = -2.3 df = 24

2.9 ± 0.38 0.8 ± 0.28 P \ 0.001

t = -7.8 df = 24

Paracoccus zealandicus

20/12/06–4/1/07 1.4 ± 0.53 0.2 ± 0.09 P \ 0.05

t = -2.6 df = 24

1.4 ± 0.45 0.2 ± 0.11 P \ 0.01

t = -3.1

df = 24

Pseudococcus longispinus

20/12/06–4/1/07 23.8 ± 4.6 4.6 ± 1.26 P \ 0.001

t = -7.7 df = 24

13.9 ± 1.14 15.0 ± 4.6 NS

t = -1.6 df = 24

17/4/08–6/5/08 14.5 ± 1.06 4.6 ± 065 P \ 0.001

t = -11.8 df = 46

19.9 ± 1.63 11.3 ± 1.44 P \ 0.001

t = -5.6 df = 49

13/1/09–27/1/09 8.2 ± 0.54 0.8 ± 0.13 P \ 0.001

t = -20.2 df = 59

7.2 ± 0.51 1.4 ± 0.27 P \ 0.001

t = -15.0 df = 59

Table 3 Parasitoids reared from sentinel Pseudococcus longispinus (Pl) on potted citrus trees exposed in the orchard and bush

habitats

Date No. Pl retrieved

from orchard

No. of mummies

(% of Pl retrieved)

Numbers of each parasitoid reared from

mummies *

No. Pl retrieved

from bush

No. of mummies

(% of Pl retrieved)

Tsyd Pvar Gadv Afusc

4/1/07 115 22 (19) 5 10 1 0 375 0

6/5/08 216 24 (11) 2 0 21 0 566 0

27/1/09 136 71 (52) 21 39 5 1 205 0

Tsyd Tetracnemoidea sydneyensis, Pvar Parectromoides varipes, Gadv Gyranusoidea advena, Afusc Anagyrus fusciventris

* parasitoids failed to emerge from 12 mummies

J. G. Charles et al.

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sentinel P. longispinus retrieved from plants placed

within the orchard or on its boundary from both

experiments, but no parasitoid was recovered from the

transect plants placed beyond the orchard boundary

into the surrounding pasture (Table 5). No parasitoid

was reared from any sentinel P. longispinus retrieved

from transect plants placed in the bush or on its

boundary. However, two species of exotic parasitoids

(T. sydneyensis and Anagyrus fusciventris) were

reared from P. longispinus recovered from potted

plant #4 placed in an isolated tree beyond the bush

margin in December 2009. This was the only occasion

that any parasitoids were reared from the bush transect

plants (Table 5).

Discussion

Natural enemies of P. longispinus

The four species of parasitoids reared from P.

longispinus from the orchard—Tetracnemoidea syd-

neyensis, Anagyrus fusciventris, Gyranusoidea adve-

na and Parectromoides varipes—have been present in

New Zealand for at least 44, 14, 44, and 47 years,

respectively (Charles 1998a, Charles 1993). Anagyrus

fusciventris has also been reared from P. calceolariae

(another pest), but the others appear to be host-specific

to P. longispinus in New Zealand where they are

common throughout the North Island, especially in

citrus orchards (Charles 1993; Charles et al. 2010).

Another exotic encyrtid, Tetracnemoidea peregrina

(Compere), which attacks younger life-stages of P.

longispinus, and which is also common in New

Zealand (Charles 1993), was notable by its absence.

Nevertheless, parasitized P. longispinus from the

orchard trees and on the potted plants were collected

on every occasion that they were sampled or deployed.

P. longispinus is the dominant exotic mealybug

species in northern New Zealand, partly because it is

highly polyphagous (Ben-Dov 1994), with many

alternative host plants in modified habitats. It is also

multivoltine, with three generations a year in the

Auckland region (Charles 1981). Although population

growth may be synchronised to plant development in

spring (especially in deciduous species), the overlap-

ping generations often lead to a stable age distribution

by mid-summer (Charles 1981), such that different

sized mealybugs are usually available for parasitism.

This can explain why several species of parasitoid,

each with preferences for different sized mealybug

hosts, are often found in exotic crops wherever P.

longispinus have established (Charles 1993; 1998b).

The four species of exotic parasitoids appeared to be

permanent residents in the orchard. The similar

percentages of parasitized mealybugs collected from

the permanent trees and the temporarily deployed

potted plants indicated that the female parasitoids

actively searched for, and efficiently located, hosts,

despite the significant reduction in numbers of sentinel

P. longispinus during the deployment periods. The

extent to which individual parasitoids dispersed within

or between trees within the orchard was not deter-

mined, but their presence on most of the plants with

sentinel mealybugs indicated that the females at least

flew regularly between plants within the confines of

the orchard habitat. ‘Presence’ from sentinel mealy-

bugs is probably more ecologically meaningful than

‘numbers reared’ because those reared may conceiv-

ably have all been offspring from a single female

exploiting a relatively high density of hosts.

By contrast, the absence of any exotic parasitoids

from similar patches of sentinel P. longispinus

deployed in the bush during the same periods provides

Table 4 Mean number of sentinel Pseudococcus longispinus

per tagged leaf (±SE) (untransformed numbers per leaf) on

potted citrus trees located outside the orchard and bush in

linear transects at start and end of experimental periods, and

test statistics for the null hypothesis of no change per leaf

(paired t test on log (count ?1) mealybugs per leaf)

Date Orchard Bush

No. at start No. at end Test statistics No. at start No. at end Test statistics

Transect 1:

9/12/09–22/12/09

10.2 ± 1.16 0.6 ± 0.24 P \ 0.001

t = -18.6 df = 49

7.6 ± 0.71 2.2 ± 0.44 P \ 0.001

t = -10.8 df = 49

Transect 2:

1/4/10–15/4/10

6.4 ± 0.37 1.5 ± 0.42 P \ 0.001

t = -15.1 df = 59

5.7 ± 0.37 0.5 ± 0.43 P \ 0.001

t = -21.1 df = 59

Field study demonstrates that exotic parasitoids of mealybugs

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convincing evidence that the exotic parasitoids present

in the orchard were not present in the bush. These data

provide ‘evidence of absence’ that cannot be achieved

by isolated, non-comparative samples of native

mealybugs in the bush (Charles and Allan 2002).

Natural enemies of native mealybugs

The naturally occurring native mealybugs in the bush

were most commonly found in late spring (Novem-

ber). The very different habitats (a more or less

uniform monoculture in the orchard and a patchy

network of different host plants and mealybug species

in the bush) meant that numbers of mealybugs found

per leaf or per minute were not directly comparable.

The natural enemies of the native mealybugs were also

uncommon, but additional specimens of Errolium sp.

and Coccophagus sp. (reared from male mealybugs

and female R. namartini respectively) collected on

native trees elsewhere in Auckland during the time-

frame of these experiments (unpublished data) sug-

gested that their presence in the bush was typical of the

region. Nevertheless, the time allocated to searches

was insufficient to catalogue the full guild of natural

enemies of mealybugs in the bush, and, despite their

known presence, native parasitoids were not reared

from any sentinel native mealybugs in the bush (or

orchard). Virtually nothing is known about the biology

of any of these parasitoids, so it may be simply that

females were not present during the trap deployments.

If the native parasitoids are univoltine then there may

be a rather narrow seasonal window for oviposition

that was missed during these experiments. Such

biological unknowns would normally make it difficult

to counter the claim that the absence of parasitism by

exotic parasitoids resulted simply from small sample

size or inadequate sampling through the year, a

problem recognised by Charles and Allan (2002).

However, no exotic parasitoids were reared from the

native sentinel mealybugs in the orchard either,

providing direct evidence that the native mealybugs

were not hosts for the exotic parasitoids known to be

present. It cannot be ruled out that some exotic

parasitoids did attack the native mealybugs in the

orchard but the failure of any to survive to adult shows

that they would not be able to develop sustainable

populations in the mealybugs’ natural habitats either.

Sentinel mealybugs to detect exotic parasitoids

outside the orchard

The orchard and bush were separated by about 500 m

at their closest point—a distance that was considered

unlikely to pose a significant spatial barrier to the

mealybug parasitoids. Small parasitoids (e.g. Mymari-

dae) regularly disperse on a scale of kilometres

between hosts (Antolin and Strong 1987). Mymaridae

are about the same size as Encyrtidae (c. 1.5 mm

long), but generally less robust, so there is no reason to

suppose that Encyrtidae are any less able to disperse.

Exotic parasitoids of P. longispinus were recovered

from within the orchard during both transects, but their

absence from the potted transect trees outside the

orchard meant that there was no evidence of continual

dispersal from the orchard. Nevertheless, the recovery

of two species from sentinel P. longispinus on a potted

plant located about 50 m from the bush boundary on

22 December 2009 (Table 5) showed that female

parasitoids were active in the space between the two

habitats, and indicated that the bush was, indeed,

exposed to immigration pressure from exotic mealy-

bug parasitoids. Whether the females that parasitized

these sentinel mealybugs had originated from the

orchard or from one or more alternative host plants in

Table 5 Numbers of sentinel Pseudococcus longispinus and parasitoids recovered from potted trees placed in linear transects from

orchard and bush sites (Fig. 1)

Date Transect No. of retrieved sentinel P. longispinus (and reared natural enemies) from numbered potted citrus plants*

#1 #2 #3 #4 #5 #6

22/12/09 Orchard 39 (6) 46 (7) – 13 (0) 15 (0) 25 (0)

Bush 85 (0) 65 (0) – 65 (12) 8 (0) 17 (0)

15/4/10 Orchard 28 (3) 25 (13) 11 (1) 2 (0) 22 (0) –

Bush 4 (0) 7 (0) 2 (0) 2 (0) 0 17 (0)

* Tree # 1–2 = in habitat; tree # 3 = on habitat boundary; tree # 4–6 = increasing distance away from habitat

J. G. Charles et al.

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the environment between the orchard and the bush is

unknown. The potted plants and sentinel hosts

provided a realistic habitat for any searching parasit-

oids in the environment. Unfortunately the data from

the transect plants were compromised to a certain

extent by the rapid reduction in numbers of mealybugs

over 14 days. The deployment period was shorter than

the parasitoid life cycle, so that the mealybugs could

not have been removed by parasitoidism. The reduc-

tions probably resulted from predation or dispersal, or

a combination of both. There were many generalist

predators in the orchard (sustained by the Orchamopl-

atus citri population), including species of spiders

(Araneae), ladybirds (Coleoptera: Coccinellidae) and

lacewings (Neuroptera: Coniopterigidae and Hemero-

biidae) which are known to feed also on mealybugs.

Many adults and immature stages of the steel-blue

ladybird Halmus chalybeus (Boisduval) were found on

the retrieved sentinel plants. Flocks of insectivorous

birds, especially silvereyes (the passerine Zosterops

lateralis (Latham)) were also regularly seen in the

area. Together, these predators probably contributed

significantly to the disappearance of sentinel mealy-

bugs especially from the more exposed plants.

Although P. longispinus showed little inclination to

move when held in a shadehouse, their exposure to the

dry sunny conditions of an Auckland summer on a

small potted tree may also have prompted dispersal to

seek a cooler environment. In any event, it is possible

that some of the lost sentinel mealybugs had been

parasitized, such that the technique underestimated the

true levels of parasitoid activity outside the orchard.

Clearly, more efficient monitoring techniques are

required to determine the characteristics of dispersal

of mealybug parasitoids. Other passive means of

collection, such as sticky traps and malaise traps for

example, are more efficient, but they collect indis-

criminately and require expertise and time to sort and

identify parasitoids of interest. A more targeted

technique may be to exploit the fact that many (but

not all) host specific parasitoids of Coccoidea are

kairomonally attracted to the sex pheromone of their

host (Dunkelblum 1999; Powell 1999). Since the trials

described above, the sex-pheromones of all three pest

species of Pseudococcus present in New Zealand have

been synthesised (Millar et al. 2005, 2009; El-Sayed

et al. 2010; Unelius et al. 2011). If the P. longispinus

pheromone proves to be sufficiently attractive to one

or more of its parasitoids then pheromone impregnated

lures may be used to much more effectively measure

their dispersal, both within and between habitats.

These data support laboratory evidence of the host

specificity of exotic Encyrtidae selected for classical

biocontrol programmes against mealybug pests in

New Zealand (Charles 1993; Charles and Allan 2002;

Charles 2011). They also provide evidence that these

parasitoids do not gradually adapt their biology and

ecology to native environments and hosts. Together,

the data support our hypothesis that New Zealand’s

native mealybugs are not threatened by exotic para-

sitoids—at least those in the Encyrtidae—even after

several decades of opportunities to exploit new

environments and non-target hosts. Similar isolation

has been recognised elsewhere. For example, eight of

the nine species of Encyrtidae introduced to Hawaii to

control pest mealybugs between 1904 and 1936 attack

only their target host, while one also attacks one other

exotic, pest mealybug (Funasaki et al. 1998). Globally,

70 % of encyrtid parasitoids of mealybugs have been

recorded from only one host, with a further 18 %

restricted to two hosts (Moore 1988). Host specificity

of these koinobiont endoparasitoids implies remark-

able co-evolutionary adaptation, and has resulted in

the success of many classical biocontrol programmes

against mealybug pests (Askew and Shaw 1985;

Moore 1988).

About 50 % of all exotic pests of New Zealand’s

fruit crops are Hemiptera, especially mealybugs

(Pseudococcidae), armoured scale insects (Diaspidi-

dae), soft scale insect (Coccidae) and aphids (Aphid-

idae) (Charles 1998a). Most of the exotic natural

enemies of these pests have also arrived accidentally,

but, judging from biocontrol programmes elsewhere,

they are not always the most effective species. As a

result, several pest Coccoidea are potential targets for

new classical biocontrol programmes. Unlike the

mealybugs, a few exotic armoured and soft scale

insects are sometimes commonly found in natural

bush habitats, but the extent to which (if at all) their

exotic natural enemies follow them is not yet known.

Further studies are required to evaluate their impact on

New Zealand’s native fauna.

Acknowledgments We thank the late Rosa Henderson,

Landcare Research, Auckland, for confirming the identity of

native mealybugs found in this study, and Tony Corbett, Plant

and Food Research, Hawke’s Bay, for preparing Fig. 1. This

paper was funded in part by New Zealand’s ‘Science Solutions

for Better Border Biosecurity (B3)’ http://www.b3nz.org.

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John Charles is a senior scientist in applied entomology, with

a focus on biological control by natural enemies of pests of

fruit crops and invasive species. He has particular interest in

the biological control of Coccoidea, especially mealybugs, and

assessing the risks to New Zealand’s native insect fauna posed

by exotic natural enemies.

J. G. Charles et al.

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Shaun Forgie is an entomologist, principal scientist for Dung

Beetle Innovations Ltd., and research associate with Landcare

Research a New Zealand Crown Research Institute. His main

research interests are biological control and the ecology and

systematics of scarabaeine dung beetles.

Asha Chhagan is a research associate who undertakes diverse

studies on the integrated pest management of fruit crop pests.

Robert Edwards was a research associate with Plant & Food

Research, and is currently working in the rural sector in the

UK.

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