Download Australian Thysanoptera – biological diversity

Blackwell Science, LtdOxford, UKAENAustralian Journal of Entomology1326-67562004 Australian Entomological SocietyAugust 2004433248257Original ArticleAustralian thripsL A Mound
Australian Journal of Entomology (2004) 43, 248–257
Australian Thysanoptera – biological diversity and a diversity of studies
Laurence A Mound
CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia.
Abstract
Studies in Australia on thrips have had extensive impacts worldwide. In behaviour, the latest definition
of eusociality is derived from work on the radiation of thrips on Acacia species in central Australia,
and these Acacia thrips also having been used to develop the concept of ‘model clades’ for analysing
the evolution of behavioural and ecological diversity. In ecology, the concept of the lack of density
dependent factors in population dynamics was elaborated through studies on the plague thrips of
southern Australia. In virology, thrips were first shown in Australia to be the vectors of tospoviruses,
although these viruses, their vectors and the plants attacked are all non-native to this continent. Work
in Australia has included the development of electronic methods of illustration, identification and
information transfer about thrips, including the use of molecular methods for pest species recognition,
and considerable advances have been made in Australia in our knowledge of the relationships between
thrips and plants, from polyphagy to pollination.
Key words
eusociality, diversity, pest recognition, thrips, virus vectors.
INTRODUCTION
The land area of Australia approximates to that of the continental USA (Fig. 1), the east–west distance from New York to
Los Angeles being about equal to that from Sydney to Perth,
and Seattle being as far from Miami as Darwin is from
Melbourne. In particular, whether from the faunistic, quarantine, or political viewpoints, it is important to remember that
Darwin is much closer to Jakarta than it is to Melbourne.
Australia thus encompasses many climates and ecosystems,
from the tropical rainforest of Cairns in the north-east and
the tropical vine thickets of Darwin and Kakadu, to the arid
areas of Central Australia, and the temperate rainforests of
Tasmania, southern Victoria, or the south-west of Western
Australia. The great size and climatic range of this continent,
together with its geographical isolation from the rest of the
world for at least 40 million years, has produced a unique and
highly diverse flora and fauna. Two plant genera, Acacia and
Eucalyptus, are known to each include about 1000 species,
some other genera each comprise several hundreds of species
(Table 1), and although the total insect fauna is currently estimated at 200 000 species (Yeates et al. 2003), this may rise to
nearer 500 000 when a greater proportion of the continent is
sampled more intensively. Superimposed onto all this is a
diverse agricultural economy, involving crops and pest insects
that have been introduced from many parts of the world. Studies on such diversity must inevitably be limited, as much by
the tyranny of distance as by the small size of the human
population and consequent financial budgets for research.
Email: [email protected]
The objective of this paper is to summarise recent studies
on the Australian members of a single order of insects, the
Thysanoptera. Historically, thrips have played a conspicuous
role in Australian entomology, considering the impact on ecological theory of the long-term population studies on Thrips
imaginis (Andrewartha & Birch 1954), and the pioneering
studies on thrips as vectors of the damaging tospovirus infections of crops (Best 1968). Recent years have seen a range of
studies on Thysanoptera in Australia that involve various biological disciplines, such as pollination, as well as other aspects
of host–plant associations, including coevolution and host capture within particular thrips lineages. Since their haplo-diploid
sex control mechanism is similar to that of Hymenoptera,
thrips have provided pivotal material in Australia leading to a
new definition of sociality amongst insects. Much of this thrips
research has derived from the availability of taxonomic expertise, a factor too often ignored when resourcing biological
studies, and work in Australia has contributed much to the
development of new technologies for routine identifications,
using electronic and molecular methods. This paper focuses
on four aspects of recent work on thrips in Australia: faunistic
studies, floristic associations, the diversity in behaviour and
biology within three particular lineages each on a different
plant genus, and investigations on pest and immigrant thrips.
FAUNISTIC STUDIES
Prior to 1900, only one endemic Australian thrips was known,
Idolothrips spectrum Haliday, the giant thrips that was apparently described from specimens collected by Charles Darwin.
Between 1925 and 1930 there was a surge of descriptive
activity with about 160 new species, but unfortunately most
Australian thrips
Fig. 1. Comparative areas of USA, Australia and the British
Isles (courtesy Helen Brookes).
Table 1 Species-rich plant genera in Australia, and associated
species of Thysanoptera, Phlaeothripinae
Plant genus
Acacia
Eucalyptus (sensu lato)
Grevillea
Eremophila
Leucopogon
Hakea
Casuarina (sensu lato)
Geijera parviflora
Plant species
Phlaeothripinae species
1200
1000
350
220
200
150
80
1
250
15
10
of these were described from single, often damaged, specimens with no biological information, and 50% are now considered synonyms. Not until after 1960 were serious attempts
made to understand the thrips fauna of Australia and its distribution and relationships to the native flora (Mound 1996).
One measure of the expanding knowledge is an increase from
445 species listed in the 1996 Australian catalogue, to over
550 listed in 2003 on the web site: http://www.ento.csiro.au/
thysanoptera/Ozthrips/Ozthrips.html. Moreover, a further 150
new species are being published during 2004 (Crespi et al.
2004; Mound 2004). More important than such numbers is the
expanding knowledge of the breeding hosts and biology of
many species, and an appreciation that Australia is a continent
of diverse ecosystems and soil types across which the thrips
fauna is by no means uniform.
As with so many Australian organisms, there appear to be
three main faunal elements; a south-east Asian fauna around
the northern and north-eastern coasts, a Bassian fauna in the
south-east, and an Eyrean fauna across much of the arid
remainder of the continent. Considering first the tropical
fauna, at least 20 species appear to be established in northern
Australia that would until recent sampling have been considered to be Oriental (Mound 2002a). For example, Thrips
unispinus was described from New Guinea, and Scirtothrips
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dobroskyi from the Philippines, but both are now recognised
as amongst the most common thrips of Australia’s north.
Although this northern tropical fauna may comprise resident
populations, the possibility exists that the populations of some
species are reinforced from Indonesian territories through
regular (or irregular) immigration on wind systems. In
contrast, several gall thrips genera, such as Euoplothrips,
Gynaikothrips and Leeuwenia, are primarily Asian, but each
has several apparently endemic species in the wet tropical
parts of Australia (Marullo 2001; Mound 2004).
The southern thrips fauna is both less species rich and less
studied, although some species are shared with territories further south. For example, Karphothrips dugdalei was described
from New Zealand but is widespread in southern Australia
on swordgrass, Gahnia (Mound 2002a), and Cartomothrips
manukae occurs on Leptospermum ericoides in New Zealand
and Tasmania. Currently, Physemothrips is known only from
Macquarie Island and southern New Zealand. More significantly, Pseudanaphothrips is an Australian endemic genus of
about 12 species primarily from the south-east, and this
appears to be a sister genus to the major South American genus
Frankliniella, these two representing independent radiations
from a Gondwanan ancestor (Mound 2002d). Indications of a
Southern Hemisphere connection are also provided by three
further genera; in the Melanthripidae, Dorythrips has two species in Western Australia and three in western South America,
and Cranothrips has one species in South Africa and at least
10 across the western half of Australia (Mound & Marullo
1998), whilst in the Phlaeothripidae, Jacotia has one species
in South Africa and at least three across southern Australia
(Mound 1995).
The Eyrean thrips fauna is more extensively sampled.
Desmothrips in the Aeolothripidae (Mound & Marullo 1998)
and Odontothripiella in the Thripidae (Pitkin 1972) are both
endemic genera that are rich in species associated with flowers, whereas living on leaves in the arid zone there are at least
30 endemic species of the worldwide genus Scirtothrips, as
well as three species shared with Indonesia (Hoddle & Mound
2003). Similarly, based on collections at Commonwealth
Scientific and Industrial Research Organisation (CSIRO),
Canberra, the worldwide genus Anaphothrips is known to
include at least 30 undescribed Australian Eyrean species, and
there is also a considerable number of species in the worldwide genus Neohydatothrips. Amongst the Phlaeothripidae,
radiation within three lineages is discussed below in the section Evolution, Host-Utilisation and Structural Diversity. In
addition to these, about 20 named and 30 undescribed species
are currently filed under Teuchothrips; these induce leaf deformation on native plants in several families widely across
Australia but rarely in the Eyrean zone. Major radiations have
also occurred amongst fungus feeding Phlaeothripidae in leaf
litter, although most species remain undescribed and the fauna
is inadequately sampled (Mound 2002b). Curiously absent
from the Australian fauna are any endemic species of the
grass-flower thrips, Chirothrips and Arorathrips, the species
of these genera recorded from Australia being introduced from
Europe, Africa or the Americas. This absence is particularly
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L A Mound
notable in view of the rich fauna of endemic thrips, mostly
undescribed, associated with Poaceae.
FLORISTIC ASSOCIATIONS
The Australian flora is very rich, with outstanding hot-spots in
particular areas (Crisp et al. 1999). However, there is no evidence that the thrips fauna correlates with this floristic diversity, either generally or locally. Thus the south-west of Western
Australia has one of the richest floras in the world, but there
is little evidence that it supports any particular thrips diversity.
Australia’s second largest plant genus, Eucalyptus (sensu
lato), comprises approximately 1000 species, but the leaves of
these myrtaceous trees and shrubs support only a single thrips,
Australothrips bicolor, itself a polyphage on Myrtaceae. In
contrast, the flowers of Eucalyptus species have three further
species, Thrips australis and T. imaginis together with their
predator Andrewarthaia kellyanus. The many plant species in
the Proteaceae support remarkably few thrips, with an occasional population of Pseudanaphothrips breeding in Banksia
flowers, some Cranothrips species apparently specific to certain white or yellow-flowered Hakea species, but not a single
species specific to the flowers of any Grevillea. Moreover,
leaf-feeding Phlaeothripidae have not been found on any
member of the Proteaceae (Table 1).
Apart from the three thrips lineages discussed in the next
main section below, few patterns of association above the
species level have been detected between thrips and plants.
The flowers of Fabaceae support members of Odontothripiella, and there remain many undescribed species from such
flowers. However within this genus, the members of one species-group are specific to the florets of native Poaceae, such
as Themeda and Stipa species, and several species in Western
Australia are apparently associated with the flowers of Asteraceae (Pitkin 1972). In the genus Pseudanaphothrips, different
species are associated with the male cones of Araucaria
(Pinopsida), the male flowers of Casuarina (Casuarinaceae),
and flowers of Cassinia (Asteraceae). Moreover in Scirtothrips, although seven species are associated with Acacia,
the other members of the genus in Australia are found on
the leaves of Casuarinaceae, Myrtaceae, Proteaceae and
Santalaceae, as well as tree ferns and cycads (Hoddle &
Mound 2003). Four gall-inducing species of the tropical
phlaeothripine genus Leeuwenia are known from Australia,
each from one species in a different plant family, Ebenaceae,
Flacourtiaceae, Grossulariaceae and Vitaceae; in contrast, nine
species of Leeuwenia are recorded from the Oriental region
on the plant genus Eugenia (Myrtaceae) (Mound 2004). Several species of Neohydatothrips that are endemic to Australia
have been taken from native Fabaceae, and at least three species of Hydatothrips occur in this country on different species
of Parsonsia vines (Apocynaceae). Species of Dendrothrips
occur on a wide range of plant families across the Old World
(Marullo 2003), but the hosts are usually trees and shrubs with
relatively hard leaves, two of the endemic Australian species
occurring only on Flacourtiaceae. Similar association with leaf
texture, rather than plant systematics, is particularly notable in
Neohoodiella jennibeardae that breeds only on the hard rugose
leaves of the monocotyledonous vine Ripogonum elseyanum
and the dicotyledonous tree Ficus coronata (Mound &
Williams 2003). Irregular and opportunistic host relationships
are thus widespread amongst Thysanoptera, and this pattern
of host exploitation contrasts with the assumption of many
entomologists that related insect taxa are likely to be associated with plant taxa that are themselves related.
Host associations in thrips are progressively being shown
to have various levels of complexity. For example, work in
other countries has demonstrated that the nitrogen status of a
plant is important in determining the population level of
Frankliniella occidentalis, whereas a related species Frankliniella fusca seems to respond to plant architecture and secondary metabolites but not nitrogen content (Brodbeck et al.
2002). In Australia, the introduced species Frankliniella
schultzei is abundant around Brisbane within the rolled petals
of the South American shrub, Malvaviscus arboreus. This
plant has thus been referred to as the ‘primary’ host of this
thrips (Milne & Walter 2000), and the other plants on which
it is found around Brisbane as ‘minor’ hosts. However in other
parts Australia, very large populations of F. schultzei occur on
a wide range of non-native plants in the absence of Malvaviscus. Not only has this species earned the common name
tomato thrips but, as discussed below, it can also function as
a useful predator of phytophagous mites on young cotton
leaves. To some extent, its host associations seem likely to be
related to its thigmotactic behaviour, that is, the habit of positioning the body with the maximum amount of surface in
contact with some other structure. This behaviour leads to this
thrips being found between the rolled petals of Malvaviscus
or within the tight florets of Trifolium, but less commonly in
more open flowers. The behavioural and nutritional stimuli
that are involved in host acceptance by thrips remain poorly
understood. Sometimes a thrips can be found in large numbers
but only on one or a few individuals of a plant species at any
one locality; such patchiness in distribution may be stochastic
or be related to physiological differences between individual
plants, but experimental evidence is lacking.
Pollination is a further aspect of thrips host plant relationships that has received attention in Australia recently.
Although the life cycle of many thrips species is dependent on
particular flowers, these insects are usually considered no
more than pollen predators. Feeding rates have been recorded
between 29 and 843 pollen grains per thrips per day, depending on the size of the pollen, with a single second instar larva
of the plague thrips, Thrips imaginis, consuming 1626 pollen
grains in one day (Kirk 1987). Despite this, evidence that plant
species may benefit from an association between thrips and
flowers is steadily increasing. For example, the Australian
eastern rainforest tree Wilkiea huegeliana has small white
flowers that are pollinated by Thrips setipennis (Williams
et al. 2001). This appears to be a specific association on the
part of the plant, although the thrips occurs in a wide range of
small white flowers in the coastal forests of much of southeastern Australia. In contrast, Cycadothrips species have been
Australian thrips
found only in the cones of Macrozamia cycads. Three species
have been described in this genus, from Macrozamia species
in western, central and eastern Australia (Mound & Terry
2001). The thrips breed only in the cycad male cones, and
populations in these have been estimated as totalling 50 000
individuals in a single cone. However, the adult thrips are
attracted to female cones for a short period when these are
mature, apparently in response to chemical signals that
are similar to those emitted by male cones (Terry 2001; Terry
et al. 2004), and the thrips have been calculated to deliver into
a female cone an equivalent of 5000 pollen grains per ovule
(Mound & Terry 2001). These observations in Australia are
entirely novel for the Cycadopsida, worldwide, and may indicate that thrips were one of the earliest insect groups involved
in pollination (Terry 2002).
EVOLUTION, HOST-UTILISATION AND
STRUCTURAL DIVERSITY
Only in Australia have evolutionary radiations of any Thysanoptera lineages been examined within the context of their
host–plant associations. However, the three radiations discussed below have been studied at very different levels. A
radiation on the single plant species Geijera parviflora has
been examined only at the level of descriptive taxonomy,
whereas behavioural observations have been made on some
members of a thrips radiation on four species of Casuarina,
and an extensive radiation involving at least 250 thrips species
on about 80 species of the genus Acacia has been studied at
various levels.
Geijera parviflora is a widespread shrub along the western
slopes of the Great Dividing Range in eastern Australia, from
north of the Queensland border to South Australia. At least 10
species of Phlaeothripinae, involving three genera, are known
only from this plant, on which one or more induces the margins of the leaves to roll into the midrib (Mound 1971). Unfortunately, the tissues of these leaf-roll galls harden rapidly, such
that it is not possible to examine the contents without totally
destroying a gall. However, the available evidence indicates
not only that several species can occur on a single plant, but
that more than one thrips species can be found in the galls on
any one leaf. Without behavioural studies it is not possible to
consider further how such a suite of closely related, but structurally divergent, species can have evolved on the leaves of a
single plant species, particularly as no related species have
been found on other plants in surrounding habitats.
The plant family Casuarinaceae includes more than 60
species in Australia, although most of these are now placed in
the genus Allocasuarina with only six in Casuarina. A few
Thysanoptera have been found on various members of Allocasuarina, but there is a remarkable radiation of Phlaeothripinae living in woody galls on four species of Casuarina. The
galls are induced by the feeding of three species of Iotatubothrips; I. kranzae on C. obesa in Western Australia, I. crozieri
on C. cristata and C. pauper in eastern Australia, and an
undescribed Iotatubothrips species on C. cunninghamiana in
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south-eastern Queensland. Each of these thrips species is polymorphic, with wingless adults differing considerably in structure from winged adults. But in I. kranzae the male genitalia
are also remarkably dimorphic (Fig. 2), the aedeagus of
winged males being almost twice as long as that of wingless
males of the same body size (Mound et al. 1998). The woody
galls are induced by these thrips on young slender branches,
but the galls continue to grow for several years, judging from
their size on older branches. These galls are frequently invaded
by two species of kleptoparasitic, phytophagous phlaeothripines, each of which also has winged and wingless adults
that differ strikingly in body structure. Despite the differences
in Casuarina gall-inducing species across Australia, the species of kleptoparasite are apparently the same in galls from the
east and the west. In one of the kleptoparasitic thrips, Phallothrips houstoni, an adult female having invaded a gall secretes
a material that forms a membrane separating a small area
within the gall, and she then produces a brood within the
security of the cell surrounded by this membrane. Her first
generation become stoutly built wingless adults (Fig. 3), very
different in structure from their gracile mother, and these then
break out of their cell and kill the original Iotatubothrips
individuals (Mound et al. 1998).
Australian species of the plant genus Acacia support a
single lineage of phlaeothripine thrips that comprises at least
250 species (Morris et al. 2002a). This suggests the remarkable evolutionary scenario that Acacia in Australia has been
invaded and adopted as a host-plant by thrips on a single
occasion. This lineage has then diversified structurally and
behaviourally on these plants, partly through the adoption of
a range of different niches, but also through varying levels of
cospeciation and host capture. No thrips taxa that could be
considered closely related to this Acacia thrips lineage have
been found on any other Australian plants. Moreover, these
thrips are not found equally across the diversity of the genus
Acacia, with most species on about 65 of the 450 species in
the phyllodinous Sections Juliflorae and Plurinerves, but with
very few on scarcely 10 of the 400 members of the Section
Fig. 2. Iotatubothrips kranzae aedeagus, wingless and winged
males.
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Fig. 3. Phallothrips houstoni wingless and winged females.
Phyllodineae (Morris & Mound 2002). Not only is there an
asymmetry in the thrips associations within the genus Acacia,
but there is a pronounced cascade effect such that a few plant
species support a large number of thrips species whereas most
of the plants involved support few thrips species (Crespi et al.
2004).
The Acacia thrips include species that are gall-inducers,
domicile-builders, kleptoparasites, and opportunistic invaders,
and this diversity of behaviours is associated with structural
differences among the thrips that are sufficiently great for
traditional morpho-taxonomists to have placed some species
in different families (Mound & Morris 2004). An initial reason
for studying the Acacia thrips was the recognition that social
behaviour had evolved amongst some of the gall-inducing
species (Crespi 1992a,b), and this led to a redefinition of the
general concept of eusociality. Previously the concept of
sociality had emphasised the importance of parental care, but
Crespi and Yanega (1995) redefined eusociality as involving
the production of a specialised morph with reduced reproductive capacity that provided some other function within a colony. Acacia gall thrips exhibit two extremes in their breeding
strategies. Some species induce large galls within which the
foundress rapidly lays up to 1000 eggs, these subsequently
giving rise to adults that are similar in structure to their parents. In contrast, other species induce small galls (Wills et al.
2001) within which the foundress lays only a few eggs, and
these give rise to wingless adults of both sexes with enlarged
forelegs and prothorax. These wingless adults function as
soldiers, fighting to protect their gall from invading caterpillars
and kleptoparasitic thrips (Crespi & Abbot 1999; Perry et al.
2002), and in some species the females have reduced reproductive capacity (Kranz et al. 2001; Chapman et al. 2002).
Phylogenetic analysis of the relationships among the 21
described species of gall-inducing thrips on Acacia has suggested that the capacity to produce soldiers arose only once
(Morris et al. 2001), and that this ability has been lost by two
species. All six members of this soldier-producing clade
induce galls only on species within the Acacia Section Plurinerves, although the significance of this, and the relationship
between sociality, soldier reproductive capacity, and the significance of kleptoparasitic thrips in driving the evolution of
soldiers remain areas of active research (Chapman et al. 2000;
Wills et al. 2004). Intraspecific wing-reduction itself is possibly a plesiotypic strategy within the Thysanoptera, since it
occurs in species in the most basal clades, and many Australian
gall-inducing thrips in lineages distinct from that on Acacia
have a short-winged morph in one or both sexes. Unfortunately there have been no investigations into the significance
of short-winged morphs in most Thysanoptera species.
The gall-inducing suite is only a small fraction of the
Acacia thrips lineage (Crespi et al. 2004), despite being the
group that has received most research attention. Species in one
structurally diverse group, involving several genera, manipulate the phyllodes of their Acacia host and then glue or sew
them together, thus creating a sheltering domicile within
which to raise a brood. Species with this type of behaviour are
found across the arid zone, with one genus including at
least six species on brigalow (A. harpophylla) in southern
Queensland, and other genera with several species on mulga
(A. aneura). One of these domicile-creating species has been
shown to exhibit the unusual behaviour of pleometrosis, that
is, colony formation involving collaboration between two or
more foundresses (Morris et al. 2002b). Females produced
subsequently within these colonies commonly have the wings
cut off just beyond their bases, but the purpose of this dealation is not known. On A. catenulata, two species have been
observed to create a domicile by weaving onto the surface of
a phyllode a membrane that forms a tent within which the
brood is then reared (Mound & Morris 2001). The structural
and behavioural diversity of these domicile-creating thrips is
great, but molecular evidence suggests that they may constitute a single lineage (Morris et al. 2002a). This evidence also
indicates that members of two genera within the lineage have
lost the ability to build their own domiciles. These species
have reverted to a presumed ancestral behaviour of being
opportunist invaders of abandoned spaces on Acacia trees,
such as old galls and empty leaf-mines.
Domicile-building thrips are also attacked by phytophagous kleptoparasitic thrips species, some of which have body
appendages that are unique to the Australian fauna. Xaniothrips species have a bizarre array of spines laterally on the
abdomen. By thrashing the abdomen vigorously, these spines
are used to drive out the original inhabitants from a domicile,
in much the same way as a porcupine uses its tail as an
offensive weapon (Mound & Morris 1999). Other presumed
kleptoparasites have unusual spade-like structures on the anterior margin of the head or on the basal antennal segments
Australian thrips
(Mound & Morris 2000). The molecular evidence indicates
that the various kleptoparasitic thrips on Acacia constitute
a single clade; that is, kleptoparasitic behaviour arose once,
and the structural diversity evolved subsequently. One species
within this lineage of kleptoparasites has evolved into a true
inquiline, in that it produces small colonies within those of the
domicile producer without usurping the space for its own use
(Morris et al. 2000).
Opportunistic invasion of small spaces on Acacia trees may
have been the plesiotypic life style within the Acacia thrips
lineage. Given the intense insolation and aridity of much of
Australia, and the ubiquity of ant predation, the ability to
occupy a small space is likely to have considerable selective
advantage. The most species-rich genera within the Acacia
thrips lineage involve such opportunistic species (Crespi et al.
2004), and the structural diversity among these thrips is
outstanding. Some groups of smaller species are associated
with naturally occurring shelters, such as splits in the younger
green branches of species such as Acacia victoriae and
A. stenophylla (Mound & Moritz 2000).
These studies in Australia constitute the most extensive
attempt yet to understand patterns of thrips evolution, host
utilisation and structural diversity (Crespi et al. 2004). The
combination of behavioural observations, coevolutionary
studies and molecular work is expanding thrips taxonomy far
beyond the descriptive response that is the usual approach to
the extensive diversity found among insect taxa.
IMMIGRANT AND PEST THRIPS
During the 19th century the Australian Acclimatisation Societies imported vast numbers of living plants and animals from
other parts of the world. This was an attempt by the colonists
to ‘enrich’ the landscapes of this continent, and also to make
these resemble landscapes of the northern hemisphere. As a
result, there are many populated parts of the continent where
Australian trees and plants are now inconspicuous elements in
the landscape. Many trees and plants were imported by sailing
ships from Europe in large wicker baskets of soil, and as a
result, many insects and weed seeds were also transported.
Considering the extent of these efforts, it remains remarkable
how many organisms failed to establish in Australia: amongst
birds, the highly popular European Robin, and amongst thrips
the abundant and widespread Thrips flavus and T. major.
Another major source of immigrant thrips species was presumably the hay and straw used for bedding and food for
live-stock (Mound 1983), because grass-living thrips such as
Aptinothrips rufus and Chirothrips manicatus are an important
element of the introduced fauna.
About 60 non-native species of thrips are established in
Australia (Mound 1996). The dominant thrips in the yellowflowered, introduced, species of Asteraceae is the Mediterranean Tenothrips frici, although the northern European Thrips
trehernei is sometimes found in Taraxacum flowers in the
south-east. The gold rush of the 1800s brought many ships
from California, and the ballast from these ships, off-loaded
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in harbour onto the appropriate ballast quays, probably introduced such litter-living fungus-feeding species as Allothrips
megacephalus and Merothrips floridensis (Mound 1983).
African species such as Chirothrips ah and C. atricorpus were
probably brought to Australia by ships that visited that continent en-route from Europe, and the whaling industry was
probably responsible for the introduction of Apterothrips apteris from the western coasts of the Americas to the southern
parts of Australia. The thrips fauna of Australia’s northern
coast remains poorly known, but the oriental rice thrips, Stenchaetothrips biformis, is widespread in Queensland, although
whether it is native, a natural invader through wind dispersal,
or inadvertently introduced through human trading is not clear.
The discovery of non-native thrips species in Australia continues to expand, with the marigold thrips, Neohydatothrips
samyunkur, in 1996, the mulberry thrips, Pseudodendrothrips
mori, in 1999, and the lily thrips, Liothrips vaneeckei, in 2001.
The rapid expansion of air transport in recent years, to include
large numbers of living plants and crops, has brought new
species to Australia, including the melon thrips, Thrips palmi,
in 1989, the western flower thrips, Frankliniella occidentalis,
in 1993, and the South African citrus thrips, Scirtothrips
aurantii, in 2001. In contrast, the Californian bean thrips,
Caliothrips fasciatus, is found regularly by Australian quarantine officers within imported navel oranges, but the species has
not yet been found alive in this country. This emphasises the
importance in distinguishing between invasion and establishment when considering immigrant species.
The presence in Australia of so many exotic species
increased the requirement for a system of recognising pest
thrips species and for distinguishing these from members of
the native fauna. This led to the production of a checklist of
Australian Thysanoptera (Mound 1996), and an illustrated
dichotomous key (Mound & Gillespie 1997). However, development at the University of Queensland of the innovative
LucID software provided an opportunity to create a new
generation of computer-driven thrips identification systems.
The initial system was provided in 1998 to the staff of the
Australian Quarantine Inspection Service, but this was later
expanded to include 180 thrips species from around the world
and illustrated with 1500 colour photomicrographs (Moritz
et al. 2001). A new version of this information and identification system includes a novel method for displaying information from ITS-RFLP analysis, using four primer pairs and five
specified restriction enzymes, for more than 50 pest thrips
species from around the world, thus facilitating the identification of individual eggs and larvae of these species (Moritz
et al. 2004b). This novel system also involves the ability to
switch between English, German and Spanish.
Western flower thrips has been the target of considerable
research effort in several state departments of agriculture in
Australia, with a particular emphasis on assessing pesticide
resistance and effectiveness, and also the value of biological
methods for controlling populations. Native anthocorid predatory bugs do not appear to have a major impact on the pest
(Cook et al. 1996), but predatory mites seem to hold greater
promise (Steiner et al. 2003), and the possibility of adding an
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L A Mound
alarm pheromone to insecticides has also been examined
(Cook et al. 2002). Although glasshouse crops were the
initial target, field crops are being increasingly attacked.
Strawberry crops near Adelaide were amongst the first highvalue crops to suffer, but the pest now affects cherries and
nectarines and is expanding in southern Queensland and
coastal Western Australia. Expansion of western flower thrips
into the cotton growing areas might affect the integrated pest
management techniques being attempted on this crop in New
South Wales.
Frankliniella schultzei and Thrips tabaci are both phytophagous species, but both of them also function as predators,
particularly against the eggs of mites (Milne & Walter 1997,
1998b). Frankliniella schultzei can cause marked feeding
damage to cotton seedlings, but if the crop is not sprayed at
this stage, this thrips subsequently becomes an effective predator of the far more harmful two-spotted spider mites (Wilson
et al. 1996), and growth by the cotton plants quickly compensates for the early season thrips damage. The feeding habits
and host relationships of these two species are complex, breeding at particular sites being particularly successful on one or
two plant species, but with a range of subsidiary hosts on
which breeding is much less successful (Milne & Walter
1998a, 2000). Currently it is not possible to know if such
opportunism occurs only in such pest thrips species, or if it is
a more general phenomenon in this order of insects (Mound
& Teulon 1995).
The first record of thrips as vectors of virus diseases was
from Australia (Best 1968), and F. schultzei, together with
Thrips tabaci, were the two species incriminated. The reasons
why scarcely 10 thrips species worldwide are vectors of
tospoviruses continue to be unclear (Mound 2002c), although
collaborative work on Frankliniella occidentalis has indicated
that part of the reason involves the proximity of the salivary
glands to the foregut during early ontogenetic stages (Moritz
et al. 2004a). The onion thrips, T. tabaci, continues to be an
important vector in Tasmania, on potatoes and lettuce crops,
but F. schultzei, the tomato thrips, was the major vector further
north in Australia until the introduction of western flower
thrips.
Studies on the mating behaviour of F. schultzei have demonstrated that males form aggregations to which females are
then attracted, apparently in response to a pheromone (Milne
et al. 2002). However, similar male aggregations have been
reported in other flower thrips, two amongst Australian native
thrips being Parabaliothrips newmani on the leaf buds of
Morton Bay Fig trees in Sydney (Gillespie et al. 2002), and
Pezothrips kellyanus on citrus leaves and fruit (Mound &
Jackman 1998), but experimental evidence concerning how
this behaviour is mediated is lacking for both species. The
second of these two, Kelly’s citrus thrips, is particularly interesting, as it is the only native Australian thrips that has become
a serious crop pest. Moreover, it is now causing problems in
several countries around the Mediterranean. For some years
this thrips was assumed to have originated in the Mediterranean area, as its placement in the Mediterranean genus Pezothrips implies, but increasing field evidence suggests that it is
an Australian endemic, although this has yet to be demonstrated unequivocally.
A second endemic species that has achieved pest status,
albeit locally, was described from southern Queensland breeding in the male cones of Araucaria, a gymnosperm tree in the
Pinopsida. This species, Pseudanaphothrips araucariae, has
subsequently been found breeding in large numbers in the
male cones of several species of introduced Pinus trees in
Queensland. The size of these populations at one site near
Cardwell in northern Queensland was so great that a local
school was forced to curtail outdoor activities daily by midmorning, as vast numbers of the thrips were causing distress
to the children, getting in their hair and food. Enormous numbers of the thrips also accumulated on the walls and ledges
inside classrooms. Thrips have been reported as causing a
public health hazard in several countries (Mound et al. 2002),
but the host shift by this species, from native Araucaria to
exotic Pinus, was particularly interesting.
Host acceptance by thrips species, as discussed above,
involves varying levels of complexity, and experimental evidence is usually lacking for even the most common species.
Entomologists sometimes assume that because a species is
polyphagous then all populations are equally likely to have the
ability to breed on all potential host plants. However, local
preferences by particular species are often noted by field entomologists, although without experimental data. For example,
onion fields in southern New South Wales support very large
populations of the highly polyphagous onion thrips, Thrips
tabaci. Samples studied from suitable weeds around these
fields contained almost no specimens of T. tabaci, although
very large numbers of Thrips imaginis were present. In various
parts of the world T. tabaci is a pest, particularly on onions,
cabbages and tobacco, but it seems that individuals are not
likely to move onto surrounding suitable hosts when an abundance of their locally preferred host is available. Experimental
studies on such host acceptance behaviour would contribute
valuable information to our understanding of thrips ecology
and also to pest control strategies. Asymmetry in host transfer
has been reported in Thrips tabaci, such that a population
could be moved readily from various plants to leeks, but not
from leeks to tobacco (Chatzivassiliou et al. 2002), and
localised host fidelity may be a partial explanation of why
Australian populations of the polyphagous South African citrus thrips, Scirtothrips aurantii, have remained on the crassulaceous weedy host mother of millions (Bryophyllum) (Hoddle
& Mound 2003). Preliminary molecular studies on Australian
populations and on South African populations both from this
plant and citrus suggest interbreeding between thrips from
different hosts at least at a low level (Morris & Mound 2004),
thus most individuals probably remain on their natal host
although the likelihood of a host shift over time remains high.
CONCLUSION
The situation in Australia with the equivocal populations of
South African citrus thrips emphasises how little is known
Australian thrips
about population structure and host acceptance in Thysanoptera. This lack of information is general across the order,
but becomes particularly important when considering pest
species since it leaves ill-defined the target of any control
measures. Taxonomic literature commonly records as ‘hostplant’ any plant species on which one or more adult thrips
have been taken. This is done without any evidence that a
thrips species is breeding on a particular plant, and thus leads
to spurious host associations. Economic entomologists and
ecologists commonly fail to consider what proportion of the
metapopulation of a species is living on plants other than their
target crop, and thus rarely estimate the extent of movement
of thrips in and out of a crop. This lack of precision in studies
on Thysanoptera appears to be associated with an assumption
that ‘thrips are thrips’ – and involves limited consideration of
any specificity in biology of different species or populations.
For example, circumstantial evidence suggests that Frankliniella schultzei is highly vagile, with populations migrating
some hundreds of kilometres, but that F. occidentalis is relatively non-vagile, any long distance movement of this pest
resulting from human behaviour; an experimental analysis of
such behavioural differences is needed to understand population fluctuations in these pests and the epidemiology of the
tospoviruses that they vector. Similarly, it is commonly
assumed that if fewer adult thrips are to be seen on a crop
shortly after applying an insecticide spray, then this is due to
mortality. However, studies in Canada (Wayne Allen pers.
comm. 2000) indicated that some agro-chemicals may act as
repellents to thrips, and, moreover, after some days of exposure to sunlight some chemicals might even act as attractants.
The existence of such behavioural effects and their significance to population studies remains largely unexplored,
although molecular methods based on microsatellites are
increasingly available for tracing the dispersal of populations.
In contrast, recent studies on non-pest thrips in Australia have
attempted to elucidate precise host relationships of many
species, the evolutionary relationships within and between
several considerable lineages of endemic thrips, and also the
congruence between distribution patterns of species and their
preferred hosts. Such studies are inevitably slow, and involve
input from many workers in different disciplines, but progressively evidence is being provided that thrips are not just
ubiquitous irritants to be sprayed with pesticides, but are
interesting organisms with many varied and complex biologies, and that Australian Thysanoptera are amongst the most
diverse and fascinating in the world.
ACKNOWLEDGEMENTS
Many Australian entomologists have contributed to these studies on thrips, including: across the tropical north, Tony Postle
at Broome, John Moulden at Kununurra, Glenn Bellis at
Darwin, Bruno Pinese at Mareeba; at Brisbane, Gimme
Walter, John Donaldson, Bronwyn Walsh, Bill Crowe; in New
South Wales, Marilyn Steiner, JianHua Mo, Lewis Wilson,
Peter Gillespie, Gerry Cassis; in Perth, Sonya Broughton,
255
David Cousins, Andras Szito, Mike Grimm; at the Waite Campus, Adelaide, Mike Keller, Greg Baker, Darryl Jackman; at
Flinders University, Adelaide, Mike Schwarz, Tom Chapman,
Brenda Kranz; in Tasmania, Margaret Williams, Lionel Hill.
Three individuals have given particularly valuable support:
Glynn Maynard at Department of Agriculture, Fisheries and
Forestry (DAFF), Alice Wells at Australian Biological
Resources Survey (ABRS) and David Morris at the Australian
National University. Funding has been provided from the
Australian Research Council through Mike Schwarz, from
ABRS, from the Australian Quarantine and Information
Service, and from DAFF. Research facilities at Canberra are
provided by CSIRO Entomology, where I am grateful for the
support of Joanne Daly, David Yeates and John La Salle.
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