ORIGINAL PAPER

Inadvertent biological control: an Australian thrips killingan invasive New Zealand tree in California

Jon J. Sullivan

Received: 13 December 2011 / Accepted: 26 July 2013 / Published online: 24 August 2013

� Springer Science+Business Media Dordrecht 2013

Abstract Transport hubs of international trade and

tourism are sites of unprecedented long-distance

dispersal of species and novel ecological interactions.

In cases of invasive plants released from their

specialist natural enemies, novel interactions with

both resident enemies and new arrivals can accumu-

late and potentially reduce weed competitiveness. I

present here one dramatic example of this, where an

invasive woody weed in southern California is being

rapidly controlled by an accidentally introduced

genus-specialist herbivorous insect. The New Zealand

native shrub/small tree, Myoporum laetum, is a long-

time popular ornamental plant in California and has

become an invasive woody weed. In 2005, a Myopo-

rum-specific thrips, Klambothrips myopori, was dis-

covered (and described) in California feeding on M.

laetum leaves. Several searches have failed to find K.

myopori in New Zealand and a population has recently

been discovered in Tasmania, Australia, feeding on

Myoporum insulare. In 5 years, K. myopori has killed

off about half of southern Californian M. laetum with

almost all surviving individuals being gradually

defoliated. Inadequate border biosecurity has resulted

in inadvertent biological control, in a rapid timeframe,

caused by a novel enemy. Unfortunately, K. myopori

has subsequently been accidentally transported from

California to Hawaii where it is now killing off

Hawaiian native Myoporum sandwicense. Transport

hubs can both connect weeds with natural enemies and

disperse those enemies more widely.

Keywords Enemy release hypothesis �Invasion biology � Myoporaceae � Plant–insect

interactions � Phlaeothripidae

Introduction

Species invasions lead to novel species interactions,

often with unexpected ecological consequences for

both native and naturalised populations (e.g. Chittka

and Schurkens 2001; Power and Mitchell 2004;

Carvalheiro et al. 2008). Novel interactions and

reunited host–enemy interactions can also accumulate

over time and potentially decrease the competitiveness

of invasive species (Hawkes 2007; Diez et al. 2010). I

describe here the unexpected, dramatic decline in

southern Californian populations of the New Zealand

endemic ngaio, Myoporum laetum (Myoporaceae), an

invasive woody weed in coastal Californian wildlands

(Bossard et al. 2000). Ngaio was one of only 13 weeds

of coastal California highlighted in the ‘‘Plant Right’’

programme of California Horticultural Invasives Pre-

vention (2005). Its rapid decline has been driven by the

accidental introduction and sustained population

J. J. Sullivan (&)

Department of Ecology, Lincoln University, PO Box 84,

Lincoln 7647, New Zealand

e-mail: sullivaj@lincoln.ac.nz;

tabebuia@alumni.upenn.edu

123

Biol Invasions (2014) 16:445–453

DOI 10.1007/s10530-013-0532-x

outbreak of a Myoporum-specific herbivorous thrips

(Mound and Morris 2007). It serves as an example of

inadvertent (fortuitous) biological control via a new

host association, and highlights both the biocontrol

opportunities and dangers of ongoing insect move-

ments via international trade.

To understand the full context and implications of

this case study, it is useful to briefly review the

invasion of its host, M. laetum, into California. As is

often the case with ornamentally sourced wildland

weeds, ngaio (also called ‘‘New Zealand myoporum’’

in California) was a popular, widely planted orna-

mental for several decades before producing invasive

wild populations. Ngaio was one of several New

Zealand woody species planted ornamentally in Cal-

ifornia by the 1860s (McClintock and Turner 2001).

New Zealand plants, including ngaio, gained sub-

stantial exposure at the Panama Pacific International

Exposition in San Francisco in 1915 (McClintock and

Turner 2001), with the associated publication of New

Zealand plants suitable for North American gardens

by Cockayne (1914).

Ngaio was widely planted in coastal California

especially throughout the 1950s to 1970s (Pool 2002;

Sullivan 2004). It was one of ‘‘a very few trees’’

planted widely along San Francisco streets in the late

1960s and 1970s (Sullivan 2004, p. 9), and in 2002 was

still the 18th most abundant street tree in that city

(Maco et al. 2003). A popular garden book of the

western USA describes ngaio as having ‘‘exception-

ally fast growth’’ and being ‘‘superb for seaside use’’

(Brenzel 1995, p. 385). Ngaio is listed among the 150

ornamental street tree species used by the City of Los

Angeles Bureau of Street Services (2009) and has been

widely planted along highways throughout southern

California (Pool 2002; Mound and Morris 2007).

While ngaio is no longer a species of choice for

highway planting (Pool 2002) or street planting in San

Francisco (Sullivan 2004), it remains an abundant

species planted throughout much of coastal California.

The great bulk of M. laetum in California is, or

originates from, the popular cultivar M. laetum

‘Carsonii’. Pressed specimens of the original San

Diego parent, collected in 1968, were lodged in the

Allan Herbarium (CHR), Lincoln, New Zealand

(specimen CHR 239205) and later determined as M.

laetum by New Zealand botanist W. R. Sykes. The

specimen label recounts that plants were bred by

Stanley R. Carson, Pacific Beach, California and

released to the trade in 1951 as Myoporum Carsonii. It

has also been listed by nurseries as M. Carsonii, M.

laetum carsonii and M. ‘Carsoni’.

Wild populations have arisen from planted ngaio

throughout much of costal California, from Sonoma

County (38� north) to San Diego county (32� north)

(Kitz 2006). It has also naturalised in the Baja

California peninsula of Mexico (Harris 1998). Ngaio

can form dense monocultures, shading out competing

plants (Kitz 2006). The accumulation of dead wood in

the interior of the plant can also be a fire risk (Bossard

et al. 2000). While being ‘‘surprisingly drought

tolerant’’ (Kitz 2006), it is predominantly found in

coastal areas, woodlands, and riparian areas (Califor-

nia Invasive Plant Council 2006), and has been a

successful invader of the few remaining coastal

wetlands of southern California (Kitz 2006). Large

plants must typically be controlled with herbicide

since ngaio resprouts after cutting or fire and its leaves

are toxic to mammals due to a furanoid sesquiterpene

ketone in the oil glands (Kitz 2006).

In 2005, an unidentified species of thrips was first

found attacking the foliage of ngaio in Orange County,

southern California (Downer 2006; Mound and Morris

2007). This species was subsequently described as

Klambothrips myopori of the Phlaeothripidae (Mound

and Morris 2007). The 44 specimens used by Mound

and Morris (2007) were collected in 2006, from three

sites in Los Angeles, Orange, and San Diego Counties.

By 2008, K. myopori had reached San Francisco Bay

area. In 3 years from its first detection, K. myopori was

present at sites spanning over 750 km, a rapid spread

rate perhaps facilitated by human dispersal of nursery

material.

Until recently, K. myopori was only known from

California, although it has an undescribed, morpho-

logically similar and molecularly distinct sibling

species in south-eastern Australia, that feeds on

Myoporum insulare (Mound and Morris 2007; Mound

2008). To date, K. myopori has been reported feeding

on M. laetum, including the popular cultivar M. laetum

‘Carsonii’, and a creeping ornamental hybrid, Myo-

porum ‘Pacificum’. Regrettably, by March 2009 it had

also now reached Hawaii where it is feeding on and

killing the Hawaiian native prostrate Myoporum

sandwicense (Conant et al. 2009). Mound and Morris

(2007) and Mound (2008) speculated that K. myopori

may be a New Zealand native species based on its

abundance on M. laetum in California. However, there

446 J. J. Sullivan

123

are no published records of herbivorous thrips feeding

on M. laetum in New Zealand (Didham and Pawson

2011; Martin 2009), and this is supported by

subsequent targeted searching (Ross Beever, Jenny

Dymock, Richard Hill, Nicholas Martin, and Jon

Sullivan, unpublished data). In 2011, after much

searching, Laurence Mound and Stephen Cameron

(CSIRO, unpublished data) discovered a population of

K. myopori feeding on M. insulare in Tasmania,

Australia (1,500 km from New Zealand).

I had the opportunity to visit a coastal area of

Orange County, southern California, eight times

between late 1997 and 2011. Ngaio is a common

plant in this area, both planted and wild. When I first

visited, the ngaio were healthy plants. By 2009, almost

all plants were infested by K. myopori and by 2011

almost half of the plants were dead. In this paper, I

describe this rapid dieback of ngaio caused by the

invasion of K. myopori. It is a dramatic example of the

unexpected ecological consequences of mixing new

species in new ranges.

Methods

Invasion and impacts of K. myopori in southern

California

In February 2009, I surveyed the extent of Klambothr-

ips defoliation on M. laetum plants at three sites in

Orange County: lower San Gabriel River area between

the East Pacific Coast Highway and State Route 22

(WGS84 33.76�N 118.09�W), Bolsa Chica Ecological

Reserve (Huntington Beach, 33.70�N 118.04�W), and

the Upper Newport Bay Nature Preserve and Ecolog-

ical Reserve (33.65�N 117.87�W). All sites are\20 m

in elevation and\7 km from the coast. In the lower San

Gabriel River area, M. laetum is the dominant woody

plant of highway roadside plantings and wild plants are

scattered in neighbouring abandoned wasteland areas.

Wild M. laetum are on the margins and higher grounds

of both wetland sites, originating from nearby

plantings.

At the first two sites, I used photos I had taken

during visits prior to 2005 to assess changes in plant

health after K. myopori arrival. For the Upper Newport

Bay site, I compared plants in 2009 with photos from

my only previous visit in January 2007, when K.

myopori herbivory was already present on some

plants. For all sites, I also compared my 2009 ground

survey data to satellite and aerial images, using dated

images from TerraServer (http://terraserver-usa.com/,

images dated 29 March 2004) and Google Earth

(http://earth.google.com/). Plants dead in 2009 but

alive in earlier satellite imagery were included in my

annual mortality estimates.

I scored all plants in the surveyed areas for

presence of K. myopori, plant height and maximum

width, and visually scored each plant for the propor-

tion of canopy shoots with live foliage, assigned to the

following categories: 100 % live foliage, 75–\100 %,

50–\75 %, 25–\50 %, [0–\25 %, and 0 %. Plants

with 0 % live canopy foliage and no live basal shoots

or suckers were considered dead. The reproductive

state (flowering or fruiting) was recorded for a subset

of 88 San Gabriel plants. In total, 313 plants were

surveyed from the San Gabriel River area, 81 plants

from the Upper Newport Bay Nature Preserve, and

four plants from the Bolsa Chica Ecological Reserve

(where weed control had removed most M. laetum

prior to 2009).

I dissected out all thrips from the shoots of two

haphazardly selected branches from two well-infested

trees, one sampled from Bolsa Chica on 19 February

2009 (85 mm 9 81 mm 9 70 mm), and the other

from the San Gabriel River area on 23 February 2009

(154 mm 9 144 mm 9 135 mm). This was done to

better assess the extent to which K. myopori feeding

was directly causing the leaf contortions and shoot

defoliation (rather than associated disease). It was

evident that the contorted shoot tips were associated

with K. myopori. To confirm this association, for a

random subset of 9 shoots (75 leaves) I counted K.

myopori per leaf and recorded the node of each leaf

and whether it was fully contorted, partially contorted,

or not contorted from K. myopori feeding. I also used

the Bolsa Chica samples to run a preliminary assess-

ment of the tolerance of K. myopori nymphs and adults

to freezing, by placing the branch that I dissected first

in a domestic freezer overnight (at about -8 �C) while

I retained another sampled branch of similar size in the

fridge. I also searched for the presence of potential

enemies of K. myopori, standardising this search in

2010 and 2011 to the most contorted leaf from each of

ten randomly selected accessible shoots from each of

the accessible 313 San Gabriel plants.

To assess the wider distribution of K. myopori on

M. laetum, in August 2011 I did a series of roadside

Inadvertent biocontrol of NZ plant by Australian insect in USA 447

123

surveys recording the presence/absence of M. laetum

and the presence/absence of partially or wholly K.

myopori defoliated plants for every mile (as measured

with the car’s odometer) along 141 miles of highway

between Upper Newport Bay in the south and La

Conchita (34.36�N–119.44�W) to the north.

Results were analysed in R (R Development Core

Team 2011) using binomial generalised linear models

(GLMs) and proportional odds models. None of the

binomial models were over-dispersed. For multivar-

iate models, presented P values are for their respective

treatments added last to the model. Data are available

from the Dryad Digital Repository at http://dx.doi.org/

10.5061/dryad.f4392.

Results

Invasion and impacts of K. myopori in southern

California

I first observed K. myopori and its distinctive leaf

contorting damage (Fig. 1) in December 2006–Janu-

ary 2007 in the three Orange County coastal sites I

visited. It was absent from the lower San Gabriel River

area and Bolsa Chica in my previous visit in Novem-

ber–December 2003 and all of my earlier visits to

these sites (January 2007 was my first visit to the

Upper Newport Bay Nature Preserve). This is consis-

tent with the earliest published records from 2005

Mound and Morris (2007). By 2009, there was

extensive M. laetum dieback through much of coastal

southern California (Figs. 2, 3, M. Hoddle, pers.

comm.). In my 141 mile roadside transect in 2011,

M. laetum was present along 76 miles. This included

54 of the 76 miles within 5 km of the coast. The plants

in every mile showed dieback consistent with Klam-

bothrips feeding, with one exception (a lone roadside

shelter belt in the middle of open farmland outside of

Oxnard). The heaviest damage and most dead trees

were along the Pacific Coast highway through Malibu.

Of the 398 plants I surveyed, 48.2 % were without

live shoots and presumed dead by 2011 and 37.8 % had

\25 % of their canopy with live shoots (Table 1). Of

the 206 plants still alive in 2011, 99 % had K. myopori

damage, 92.3 % with K. myopori damage on more

than 75 % of their live shoots. Almost no heavily

defoliated plants (\25 % of canopy with live foliage)

Fig. 1 Typical views of M. laetum canopies infested with K. myopori

2002 2004 2006 2008 2010

0.0

0.2

0.4

0.6

0.8

1.0

Year

Pro

port

ion

of p

lant

s

Plants alive

>50% shoots alive

>50% shoots with Klambothrips

Fig. 2 The decline in M. laetum associated with K. myopori

invasion at three sites in Orange County, California

448 J. J. Sullivan

123

were flowering or fruiting (binomial GLM comparing

with less defoliated plants and accounting for variation

in plant volume: df = 1.58, deviance = 4.5, residual

deviance = 63.9, P \ 0.05). In the San Gabriel River

area, only 12 % of plants with\25 % of their canopy

with live shoots were reproductive, while 45 % of the

plants with [50 % of their canopy with live shoots

were reproductive.

Plant size in the San Gabriel River area, as

measured by estimated canopy volume, influenced

the extent of defoliation (proportional odds model,

volume model compared with intercept only model:

df = 1, likelihood ratio = 16.45, P \ 0.001). Larger

plants were also least likely to be dead (binomial

GLM: df = 1.125, deviance = 28.5, residual

deviance = 146.2, P \ 0.001). However, many large

trees were still among the dead, with 32.3 % of trees

over 4 m high dead and of the remaining large live

trees, 33.3 % had \25 % of their canopy with live

shoots (N = 62).

While mortality was generally high, it did differ

among sites. By 2011, mortality was lower at the

Upper Newport Bay Nature Preserve (38.3 %) than in

the San Gabriel River area (51.1 %) (Table 1, bino-

mial GLM: df = 1.392, deviance = 4.3, residual

deviance = 541.5, P \ 0.05). The cause of this

difference is unclear. The Upper Newport Bay Nature

Preserve had a higher proportion of younger, wild

plants than the San Gabriel River area, which was

dominated by old highway plantings (although in

Fig. 3 Three plants photographed before and after the effects of

sustained heavy K. myopori herbivory. The upper plant was

photographed near State Route 22 in the lower San Gabriel

River area, initially prior to the arrival of K. myopori. The lower

two plants were photographed in the Upper Newport Bay,

initially shortly after the arrival of K. myopori

Inadvertent biocontrol of NZ plant by Australian insect in USA 449

123

many cases the origin of plants was uncertain). There

was very little recruitment over this same period and

seedlings (and root suckers) were as heavily damaged

by Klambothrips as larger plants.

Curiously, two nearby San Gabriel plants remained

almost entirely undamaged by K. myopori throughout the

surveys, despite being within 160 m of defoliated and

dead plants. The reproductive and vegetative characters

fell within the morphological variation of the local

M. laetum. One of the two plants, especially, sustained

scale insect colonies guarded by thousands of ants.

The branch dissections revealed the extent of the K.

myopori outbreak on M. laetum. The dissected San

Gabriel River area branch end contained 176 K.

myopori adults, 312 nymphs, and about 2,700 eggs,

from just 92 leaves, 78 of which were contorted from

thrips feeding. The Bolsa Chica branch end contained

21 K. myopori adults, 134 nymphs, and at least 256

eggs, from 105 leaves, 82 of which were contorted

from thrips feeding. Only 33 other individual inver-

tebrates were found from the two samples, including

12 black aphids from two leaves, 7 ants, 9 soft scales

from 5 leaves, one mite, one mealy bug, and one small

beetle. Mark Hoddle (unpublished data) has found a

low incidence of predatory pirate bugs (Orius sp.,

Hemiptera, Anthocoridae) and green lacewing larvae

(Neuroptera, Chrysopidae) from galled leaves at

Riverside. The overnight freezing killed all K. myo-

pori adults and nymphs in the Bolsa Chica sample

while all adults and nymphs from the refrigerated

control branch survived.

I estimated with Photoshop that the sampled San

Gabriel River area tree (5.5 m high, 8 m wide) had at

least 2,200 branch ends of the size I sampled. All

branch ends on the tree had leaves contorted by K.

myopori feeding, almost all still with live foliage

(placing it in the 75–\100 % live foliage category).

Extrapolating my counts from the one dissected

branch end gives a rough estimate of over a million

K. myopori adults and nymphs and over 5 million eggs

on this one tree. While an uncertain estimate, it

underscores K. myopori feeding as a sufficient sole

cause of the canopy dieback.

Both K. myopori individuals and damage were

concentrated on the apical leaves of shoots (Binomial

GLM of K. myopori presence: df = 1.72, devi-

ance = 21.5, residual deviance = 76.2, P \ 0.001;

K. myopori damage: df = 1.72, deviance = 6.4,

residual deviance = 73.7, P \ 0.05). Over half

(55 %) of the leaves had K. myopori adults, nymphs,

or eggs present, and most leaves were partially (19 %)

or fully (72 %) contorted. The upper three leaves of

shoots had 80 % of the K. myopori nymphs and adults

and only 19 % of the partially or undamaged leaves

(with shoots having 4–12 leaves, mean 8.3). It is

unclear whether the lower probability of K. myopori

damage to basal leaves in these February 2009

samples reflects a seasonal fluctuation in K. myopori

abundance or whether these lower leaves pre-date K.

myopori arrival on these trees. Adults and nymphs of

K. myopori were still present feeding in August 2010

(and 2011), suggesting the latter.

Discussion

This is certainly not the first case of dramatic

ecological consequences resulting from a novel com-

bination of insect herbivore and host plant, both

unintentional (e.g., Elkinton and Liebhold 1990; van

Epenhuijsen et al. 2000; Stadler et al. 2006) and

through classical biological control (e.g., McFadyen

1998; Carruthers et al. 2011). However, these are

typically of invasive insects meeting new host plants

in the plants’ native ranges, or of natural enemies

being reunited with their host plants in new ranges.

Myoporum laetum meeting K. myopori is a case of a

genus-specialist insect herbivore meeting a new

species of its host genus in a new environment. It

clearly illustrates the potential impact of new

Table 1 The percentage of plants in different canopy defoli-

ation categories in summer 2011 at two sites in Orange County,

southern California (N = 313 plants from the San Gabriel

River area between the East Pacific Coast Highway and State

Route 22, and N = 81 from the Upper Newport Bay Nature

Preserve and Ecological Reserve)

Defoliation (%) San Gabriel (%) Newport Bay (%)

0–\25 14.8 35.8

25–\50 5.5 11.1

50–\75 9.3 2.5

75–\100 14.3 12.3

100 56 38.3

Past photographs and Terraserver satellite images show that all

these plants were alive and healthy in 2004, in the 100 % or

75–\100 % categories. All live plants except for one Newport

Bay plant had K. myopori damage, usually throughout the

canopy

450 J. J. Sullivan

123

associations between herbivores with host plants, as

has been demonstrated by some classical control

programmes (e.g., Zimmermann et al. 2001; van

Klinken et al. 2003; McConnachie et al. 2004). It is

also hard to imagine how it could have been predicted

that a previously unknown and uncommon Tasmanian

insect would cause a mass dieback of a New Zealand

native plant in California.

It is perhaps notable that this meeting occurred in

southern California, a major hub of international trade

more than 12,800 km away from the native range of

both species, and not in New Zealand, 1,500 km away

from Tasmania, where M. laetum is endemic and the

original host of K. myopori, M. insulare, is planted

ornamentally and has naturalised (Webb et al. 1988).

Also notable is New Zealand’s much stricter biosecu-

rity legislation and border biosecurity procedures

(Williams 2000) than California and most of the

Pacific Island nations. The fact that K. myopori has

already moved from California to Hawaii, a 2,390 km

jump, suggests that K. myopori is more likely to reach

other Myoporum species in the Pacific from California

and not Tasmania. This echoes a similar result with

fire ants (Solenopsis invicta), where all of the world’s

invasive populations are descendants of the original

North American invasion and not multiple escapes

from South America (Ascunce et al. 2011).

Several outstanding natural history mysteries

remain. It is very unusual for a thrips population to

sustain a multi-year, large scale outbreak (Laurence

Mound, pers. comm.). Is the sustained K. myopori

outbreak in California caused by some feature of

California’s coastal environment (e.g., mild winters),

the condition of the host plants in California (e.g., heat

stress, low genetic diversity, particularly susceptible

genetic material), or the absence of specialist natural

enemies of K. myopori? The presumably low genetic

diversity in M. laetum ‘Carsonii’ combined with an

environment warmer and drier than the native range in

New Zealand could plausibly benefit K. myopori.

However, initial indications are that K. myopori

populations are also starting a sustained outbreaking

in Hawaii on native, and presumably more genetically

diverse, M. sandwicense, and plants are again being

defoliated and killed (Cythia King, Department of

Land and Natural Resources, pers. comm.). It is also

unclear why local southern California natural enemies

have not responded to the sustained K. myopori

outbreak. There is no indication yet that predatory

insects have increased in numbers on M. laetum at my

Orange County sites (personal observation). Perhaps

K. myopori exploits in some way the chemical

defences of M. laetum.

This also appears to have been an unusually fast-

acting, albeit inadvertent, case of classical biological

control. Successful weed biocontrol agents typically

take a decade or more from introduction to control a

host population, if at all (McFadyen 1998; Carruthers

et al. 2011). While it is impossible to rule out some

undetected lag phase in the case of Klambothrips in

southern California, its subsequent rapid expansion

through California and apparently immediate outbreak

in Hawaii are consistent with little to no lag.

This case is consistent with the New Associations

hypothesis (Hokkanen and Pimentel 1989; Parker and

Hay 2005; cf. Waage et al. 1988), where the combi-

nation of a genus-specialist with a naive host congener

results in particularly strong host suppression. In

classical biological control, agents are instead typi-

cally selected from surveys of natural enemies of the

weeds in their native ranges (McFadyen 1998). The

case of M. laetum and K. myopori would support the

New Associations hypothesis if it could be shown that

M. laetum is less tolerant of K. myopori herbivory than

its native host, M. insulare.

Lastly, steps need be taken to limit the further

spread of K. myopori to native Myoporum populations

beyond Hawaii. This also most likely applies to the

undescribed, closely related, Klambothrips from M.

insulare on mainland Australia (Mound and Morris

2007; Mound 2008). Internal and between state trade

in plant material by the North American horticultural

industry is almost certainly responsible for K. myopori

spreading 750 km from San Diego to San Francisco in

just 3–4 years and then to Hawaii. Klambothrips

myopori almost certainly reached California on live

Myoporum tissue imported by the horticultural indus-

try. To protect native Myoporum populations, it is

important that future movements of live Myoporum

tissue between countries are done with great care with

only seed, or, preferably, not at all.

Given that international trade is extensive and

current biosecurity procedures are inadequate to

prevent new incursions, it is perhaps inevitable that

many invasive plants will be gradually reunited with

old host-specialist enemies as well as discovered by

new enemies (Hawkes 2007; Diez et al. 2010). Many

tens of thousands of plant species have been moved

Inadvertent biocontrol of NZ plant by Australian insect in USA 451

123

from their native ranges into cultivation throughout

the world and a substantial minority continue to

naturalise. Enemy release is one important component

causing some of these plants to become invasive

weeds. In this context, the threat from ‘‘leaky’’

national borders to agriculture, forestry, and native

species will be offset to some extent by the benefits of

weeds being (re-)connected with host-specialist ene-

mies. Cases like M. laetum and K. myopori, of a genus-

specialist encountering and biologically controlling a

novel host congener in a foreign range, may become

more frequent in the future, especially in areas of the

world with heavy trade and insufficient border

biosecurity.

Acknowledgments Ross Beever, Jenny Dimock, Laura Fagan,

Richard Hill, Nicholas Martin, and Walter Stahel provided useful

information about the absence (so far) of K. myopori records from

New Zealand. Laurence Mound, Mark Hoddle, and Richard Hill

made useful comments on earlier drafts and were generous in

sharing their observations of K. myopori. Cythia King shared

useful information about the ongoing invasion of K. myopori in

Hawaii. Thanks to Stan and Helen Molles for hosting my family

and me when in Orange County.

References

Ascunce MS, Yang CC, Oakey J, Calcaterra L, Wu WJ, Shih CJ,

Goudet J, Ross KG, Shoemaker D (2011) Global invasion

history of the fire ant Solenopsis invicta. Science

331(6020):1066–1068

Bossard CC, Randall JM, Hoshovsky MC (2000) Invasive plants

of California’s wildlands. University of California Press,

Berkeley

Brenzel KN (1995) Sunset western garden book, 40th edn.

Sunset Publishing Corporation, Menlo Park

California Horticultural Invasives Prevention (2005) Plant right,

keep invasive plants in check. California Horticultural In-

vasives Prevention, California. http://www.plantright.org/

plants/invasive.php?invPlan-

tID=25&region=south\s\do5(c)oast. Viewed 19 Feb 2009

California Invasive Plant Council (2006) Plant profiles: Myopo-

rum laetum. California Invasive Plant Council, California.

http://www.cal-ipc.org/ip/management/plant\s\do5(p)ro-

files/Myoporum\s\do5(l)aetum.php#proc. Viewed 20 Feb

2009

Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin

L, Smith L, Wagner DL (2011) Classical biological control

for the protection of natural ecosystems. Biol Control

54(Suppl 1):S2–S33

Carvalheiro LG, Buckley YM, Ventim R, Fowler SV, Memmott J

(2008) Apparent competition can compromise the safety of

highly specific biocontrol agents. Ecol Lett 11(7):690–700

Chittka L, Schurkens S (2001) Successful invasion of a floral

market. Nature 411:653

City of Los Angeles Bureau of Street Services (2009) Urban

forestry division street tree selection guide. City of Los

Angeles Bureau of Street Services, California. http://www.

lacity.org/BOSS/UrbanForestryDivision/StreetTreeSelection

Guide.htm. Viewed 20 Feb 2009

Cockayne L (1914) New Zealand plants suitable for North

American gardens, with hints as to their cultivation. John

Mackay, Government Printer, Wellington

Conant P, Hirayama CK, Lee MI, Young CL, Heu RA (2009)

Naio thrips, Klambothrips myopori Mound & Morris

(Thysanoptera: Phlaeothripidae). New Pest Advisory No.

09-02, Plant Pest Control Branch, Division of Plant

Industry, State of Hawaii Department of Agriculture,

Honolulu, USA

Didham R, Pawson S (2011) BUGZ bibliography of New Zea-

land terrestrial invertebrates online, New Zealand. http://

www.bugz.org.nz. Viewed 4 Oct 2011

Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan

RP (2010) Negative soil feedbacks accumulate over time

for non-native plant species. Ecol Lett 13(7):803–809

Downer J (2006) New thrips pest attacks Myoporum. Landsc

Notes (University of California/Ventura County) 19(3):1

Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy

moth in North America. Annu Rev Entomol 35:571–596

Harris G (1998) Invasive New Zealand weeds: our native plant

invaders. CalEPPC News (California Exotic Pest Plant

Council) 6(4):8–9

Hawkes CV (2007) Are invaders moving targets? The generality

and persistence of advantages in size, reproduction, and

enemy release in invasive plant species with time since

introduction. Am Nat 170(6):832–843

Hokkanen HMT, Pimentel D (1989) New associations in biological

control: theory and practice. Can Entomol 121(10):829–840

Kitz J (2006) Myoporum laetum. In: Bossard CC, Randall JM,

Hoshovsky MC (eds) Invasive plants of California’s wild-

lands. University of California Press, Berkeley, pp 246–248

Maco SE, McPherson EG, Simpson JR, Peper PJ, Xiao Q (2003)

City of San Francisco, California street tree resource

analysis. Center for Urban Forest Research, Pacific

Southwest Research Station, USDA Forest Service, Davis,

CA

Martin N (2009) Plant-SyNZ�. Plant and Food Research,

Auckland, New Zealand. http://www.crop.cri.nz/home/

plant-synz/index.php. Viewed 4 Oct 2011

McClintock E, Turner RG (2001) The trees of golden gate park

and San Francisco. Heyday Books, San Francisco

McConnachie AJ, Hill MP, Byrne MJ (2004) Field assessment

of a frond-feeding weevil, a successful biological control

agent of red waterfern, Azolla filiculoides, in southern

Africa. Biol Control 29(3):326–331

McFadyen REC (1998) Biological control of weeds. Annu Rev

Entomol 43:369–393

Mound LA (2008) Identification and host associations of some

Thysanoptera Phlaeothripinae described from Australia

pre-1930. Zootaxa 1741:41–60

Mound LA, Morris DC (2007) A new thrips pest of Myoporum

cultivars in California, in a new genus of leaf-galling Aus-

tralian Phlaeothripidae (Thysanoptera). Zootaxa 1495:35–45

Parker JD, Hay ME (2005) Biotic resistance to plant invasions?

Native herbivores prefer non-native plants. Ecol Lett

8(9):959–967

452 J. J. Sullivan

123

Pool B (2002) Some object to Caltrans’ re-greening of freeways.

Los Angeles Times 6 June: B1

Power AG, Mitchell CE (2004) Pathogen spillover in disease

epidemics. Am Nat 164:S79–S89

R Development Core Team (2011) R: A language and envi-

ronment for statistical computing. R Foundation for Sta-

tistical Computing, Vienna, Austria. http://www.R-project.

org/. ISBN 3-900051-07-0

Stadler B, Muller T, Orwig D (2006) The ecology of energy and

nutrient fluxes in hemlock forests invaded by hemlock

woolly adelgid. Ecology 87(7):1792–1804

Sullivan M (2004) The trees of San Francisco. Pomegranate,

California

van Epenhuijsen CW, Henderson RC, Carpenter A, Burge GK

(2000) The rise and fall of manuka blight scale: a review of

the distribution of Eriococcus orariensis (Hemiptera:

eriococcidae) in New Zealand. N Z Entomol 23(1):67–70

van Klinken RD, Fichera G, Cordo H (2003) Targeting bio-

logical control across diverse landscapes: the release,

establishment, and early success of two insects on mesquite

(Prosopis spp.) insects in Australian rangelands. Biol

Control 26(1):8–20

Waage JK, Greathead DJ, Brown R, Paterson RRM, Haskell PT,

Cook RJ, Krishnaiah K (1988) Biological control: chal-

lenges and opportunities [and discussion]. Philos Trans R

Soc Lond B Biol Sci 318(1189):111–128

Webb CJ, Sykes WR, Garnock-Jones PJ (1988) Flora of New

Zealand volume IV. Naturalised pteridophytes, gymno-

sperms, dicotyledons. Botany Division, Department of Sci-

entific and Industrial Research, Christchurch, New Zealand

Williams JM (2000) New Zealand under siege: a review of the

management of biosecurity risks to the environment. Office

of the Parliamentary Commissioner for the Environment,

Wellington

Zimmermann HG, Moran VC, Hoffmann JH (2001) The

renowned cactus moth, Cactoblastis cactorum (Lepidop-

tera: Pyralidae): its natural history and threat to native

Opuntia floras in Mexico and the United States of America.

Fla Entomol 84(4):543–551

Inadvertent biocontrol of NZ plant by Australian insect in USA 453

123