Biological Control 26 (2003) 8–20
www.elsevier.com/locate/ybcon
Targeting biological control across diverse landscapes:
the release, establishment, and early success of two insects on
mesquite (Prosopis spp.) insects in Australian rangelands
Rieks D. van Klinken,a,* Gio Fichera,b and Hugo Cordoc
a
CSIRO Entomology, Tropical Ecosystems Research Centre, PMB 44 Winnellie, Northern Territory 0822, Australia
b
CSIRO Entomology, 120 Meiers Rd, Indooroopilly, Brisbane 4068, Australia
c
United States Department of Agriculture, South American Biological Control Laboratory, Buenos Aires, Argentina
Received 2 November 2001; accepted 18 June 2002
Abstract
Biological control agents are frequently expected to perform over a wide geographic and climatic range, or to target high priority
regions with specific climates. Biological control of mesquite (Leguminosae: Prosopis spp.) in Australia is one such example.
Mesquite is widely distributed across Australia, but is currently a more serious weed in some areas than others. We document the
mass-rearing, release, and establishment of two new biological control agents native to the same region in north-west Argentina. We
also determine whether climate-matching, a frequently used method for helping identify well-adapted agents, would have predicted
establishment and relative performance of each agent. Release and evaluation sites were selected to represent the diverse climates in
which mesquite is a serious weed. One insect, the leaf-tier Evippe sp. #1 (Lepidoptera: Gelechiidae), established widely. Densities of
this species were highest in the warmest region, which was 4.7 °C hotter than the point of origin, and low where climate is most
similar to the point of origin. Significant impact from Evippe sp. is likely in the warmest region (Pilbara, WA), but was not assessed
quantitatively. In contrast, the other insect, the psyllid Prosopidopsylla flava, is only tenuously established at the two coolest sites,
one of which was climatically most similar to the point of origin. Both climate and ant predation probably play a role in the failure
of psyllids to reach damaging densities, and to become established at other sites. Climate of the areas where the insects were collected
in their native range was therefore a poor predictor of performance of at least one of these two insects. Techniques other than
climate-matching are therefore required to improve our prediction of relative performance at the regional level.
Ó 2002 Elsevier Science (USA). All rights reserved.
Keywords: Prosopis; Leguminosae; Biological control; Prosopidopsylla flava; Psyllidae; Evippe sp. #1; Gelechiidae; Agent prioritization; Ant
predation; Climate-matching; Climate-modeling; Argentina; Australia
1. Introduction
Weed species often grow across diverse geographic
conditions, in both their native and introduced ranges.
Likewise, biological control agents typically perform
better in some parts of the weedÕs range than others,
depending in part on their climatic requirements. For
example, Cullen (1996) found that climatic factors explained why more than half of the 25 agent:weed combinations under consideration resulted in control in one
*
Corresponding author. Fax: +61-(0)-8-8944-8444.
E-mail address: [email protected] (R.D. van Klinken).
region and not in another. Different approaches for
considering the climatic requirements of individual insects or pathogens are available, including day–degree
modeling (e.g., McClay and Hughes, 1995) and climatemodeling that incorporates climate-related growth, reproduction, and mortality factors (e.g., Julien et al.,
1995). Data for each insect or pathogen is obtained from
laboratory studies and/or knowing the limits of the insectsÕ distribution within the native range (and parts of
its introduced range). These techniques have been used
to identify areas within the native range that might have
‘‘strains’’ of an existing agent that are better adapted
climatically (McClay and Hughes, 1995), to help design
release programs, and as a valuable tool in explaining
1049-9644/02/$ - see front matter Ó 2002 Elsevier Science (USA). All rights reserved.
PII: S 1 0 4 9 - 9 6 4 4 ( 0 2 ) 0 0 1 0 7 - X
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
the regional success or failure of existing agents (Julien
et al., 1995; McClay, 1996; McClay and Hughes, 1995;
McFadyen, 1987; Scott, 1992; Scott and Yeoh, 1999).
However, climate-modeling has not, as yet, been used
for prioritizing agents, probably because sufficient data
is rarely available, or is perceived to be difficult and
costly to obtain (McClay, 1996).
An alternative approach to identifying climatically
adapted agents is ecoclimatic matching of the native and
introduced range of the target weed (Wapshere, 1993;
Wapshere et al., 1989). This method assumes that the
most climatically adapted agents will come from parts of
the native-range that are most climatically similar to the
target range. Various methods are used to locate
matching climates within the native range, including
klimadiagrams (Dennill and Gordon, 1990; Wapshere,
1974, 1983, 1993) and more quantitative climatematching using the computer program CLIMEX (Adair
and Scott, 1997; Kleinjan and Scott, 1996). The potential limitation of this approach is that it does not account for climatic requirements of individual insects.
However, it remains the primary means by which climatic requirements are accounted for when prioritizing
potential agents (e.g., Gillett et al., 1991: Sida species;
Harley et al., 1995: Mimosa pigra L.; Marohasy, 1995:
Acacia nilotica (L.) Willd. ex Del.; DeLoach et al., 1996:
Tamarix species), and is widely recommended as a
coarse scale approach (Cameron et al., 1993; Sutherst
et al., 1999). In this paper we document results of this
approach for two new agents released against mesquite
in Australia.
Mesquite (Prosopis spp.) is an example of a weed that
is particularly widespread in both its native and introduced ranges. It is a long-lived woody legume that can
form impenetrable thickets. At least four species and
several hybrids are represented in Australia, but available evidence suggests that herbivores do not discriminate between taxa (Cordo and DeLoach, 1987; van
Klinken, 2000; van Klinken and Heard, 2000). In its
native range, mesquite is present in semiarid to arid
regions from southern North America through to South
America (van Klinken and Campbell, 2001). In Australia it grows under climatically diverse conditions,
with mean annual daily temperatures ranging from 10 to
15 °C in the south to over 25 °C in the north. Mean
annual rainfall ranges from 150 to 1200 mm, and might
fall evenly throughout the year, or predominantly in
either winter or summer (van Klinken and Campbell,
2001).
A biological control program targeting mesquite in
Australia was renewed in 1994 (van Klinken and
Campbell, 2001). Potential agents were prioritized primarily on the basis of likely host-specificity and the type
and extent of damage observed in the native range
(Cordo and DeLoach, 1987; T. Heard, CSIRO Entomology, Brisbane, Qld, unpublished). Climate was not
9
considered beyond a general requirement for insects to
be adapted to semiarid or arid conditions. Two of the
four insect species tested, a leaf-tying moth and a psyllid, were sufficiently host-specific and were subsequently
released from 1998 (van Klinken and Campbell, 2001).
Both originate from the same region in northwest Argentina.
In this paper we document the mass-rearing, release,
establishment, and early performance of the two new
biological control agents of mesquite. Both agents were
released and evaluated within regions representing the
diverse climatic conditions in which mesquite is a serious
weed. Relative performance across Australia was then
compared a posteriori with predictions from climatematching to determine whether predictions from climate-matching are sufficiently accurate to guide agent
prioritization in Australian rangelands.
2. Materials and methods
2.1. Overview of the agents
Two agents were released, the leaf-tier Evippe sp. #1
(referred to as ‘‘Evippe’’) (Lepidoptera: Gelechiidae)
and the sap-sucker Prosopidopsylla flava Burkhardt
(Hemiptera: Psyllidae). Both agents are native to
northern and central Argentina. P. flava is widely distributed and has been recorded from ten provinces
(Catamarca, Chaco, C
ordoba, Formosa, La Rioja,
Mendoza, Santiago del Estero, San Juan, San Luis, and
Salta) (Burckhardt, 1987; D. Burckhardt, Naturhistorisches Museum, Basel, Switzerland, personal communication 1997/8; H. Cordo, unpublished). Gelechiid
leaf-tiers are also widespread in both Argentina and
Paraguay (Cordo and DeLoach, 1987), but few have
been reliably identified. The presence of Evippe sp. #1
has been confirmed in La Rioja and Santiago del Estero
Provinces. The mesquite taxa in Australia do not occur
naturally in Argentina (van Klinken and Campbell,
2001), and are therefore new associations for both
agents. In laboratory studies, both agents perform
equally well on all Australian mesquite taxa on which
they have been tested (van Klinken, 2000; van Klinken
and Heard, 2000).
2.1.1. Evippe
Eggs are oviposited directly onto the plant where they
are mostly placed into cracks and fissures in the bark.
Evippe has four larval instars (van Klinken and Heard,
2000). The first instar mines leaves and subsequent instars construct leaf-ties from opposing and adjacent
pinnules in which they feed. Larvae pupate in the third
and final leaf-tie. Under controlled conditions (27 °C
day, 23 °C night; 60 10% RH; L:D 16:8 photoperiod
plus limited oblique natural lighting) egg to adult
10
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
development takes between 34 and 48 days. Adults are
quite short-lived, rarely surviving for more than three
weeks. Oviposition begins within a day of emergence
and continues through the femaleÕs life, although 77% of
eggs are oviposited in the first week. Fecundity is at least
75 eggs.
Evippe diapause as fourth instar larvae (van Klinken,
unpublished). Diapause is thought to be initiated primarily by changes in daylength, as it is entered independently of temperature and moisture conditions, and
can be prevented through the use of grow lamps (see
below). In the field, larvae enter diapause in late March
or early April and exit it in July. The timing of diapause
appears to be independent of latitude.
2.1.2. Prosopidopsylla flava
Prosopidopsylla flava remains dependent on its host
throughout its lifetime (van Klinken, 2000). Each egg
has a peduncle which is inserted into the plant tissue on
which it depends for survival. Both adults and nymphs
feed on sap in mature and immature foliage. Nymphs
are relatively sedentary and adults depend on the host
plant for both egg production and survival (in the laboratory adults rarely survive more than four days in the
absence of a host plant). Under controlled conditions
(27 °C day, 23 °C night; 60 10% RH; L:D 16:8 photoperiod plus limited oblique natural lighting) development from egg to adult takes between 36 and 70 days
(median 46 days), and adults live for an average of 20
days, although individuals can live for over 56 days.
Lifetime fecundity averages about 232 eggs per female
(individuals oviposit up to 523 eggs). Oviposition commences three to five days after adult emergence and
continues relatively constantly through the femaleÕs life.
There is no evidence of diapause, at least under conditions encountered during winter in subtropical Brisbane
when mean monthly temperatures are 9.5–20.6 °C.
However, egg and nymphal development times are slowed considerably.
2.2. Release sites
Mesquite is currently a serious weed in six different
parts of Australia, referred to here as regions. One or
more mesquite infestations for direct releases were selected within each region (Fig. 1). The targeted infestations at these sites differed in species composition, size,
and density of mesquite (Table 1).
Each region (as represented by the infestation at
which most releases were made) had different climatic
conditions, which also differed from the native range of
both agents (Fig. 2). Temperatures at the point of origin
were warmer than northwest New South Wales for
much of the year and cooler than other regions for most
or all of the year (Fig. 2A). The Pilbara was hottest for
most of the year (January–July), although the Barkly
Tableland was considerably hotter from October to
December.
Fig. 1. Release sites for Evippe (up-right triangle) and/or Prosopidopsylla flava (upside-down triangle). The main release site/s within each region are
named, others are just indicated by a symbol.
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
11
Table 1
Description of infestations in which direct releases of Evippe sp. #1 and/or P. flava were made
Infestation
Latitude
Taxonomy
Size and density
North-west New South Wales (nw NSW)
White Leeds Station
32°01:9800 S
One Tree Station
30°04:1190 S
141°22:9160 E
141°55:8330 E
P. velutina Wooton
P. velutina P. glandulosa
Torr. var. torreyana
50 ha dense; >1000 ha sparse
>1000 ha isolated plants
South-west Queensland (sw QLD)
Comongin
26°29:6720 S
144°19:4080 E
P. velutina P. glandulosa
Torr. var. torreyana
4000 ha dense; 8800 ha sparse
North Queensland (n QLD)
Hughenden
Hampden downs
Moorooka Station
20°49:5240 S
21°30:5690 S
21°28:9640 S
144°12:2480 E
141°41:0200 E
141°13:1480 E
21,000 ha dense to sparse
2000 ha dense; 18,000 ha sparse
10,000 ha dense to sparse
21°16:5230 S
141°17:2450 E
P. pallida (Willd.) Kunth
P. pallida
‘‘Hybrid’’ (possibly
P. glandulosa var. torreyana)
As for Moorooka
Barkly Tablelands, Northern Territory
Alroy Downs
19°17:2500 S
Austral Downs
20°29:5220 S
Lake Nash Station
20°57:7630 S
136°04:9520 E
137°46:0670 E
137°54:7060 E
P. pallida
P. pallida
P. pallida
10,000 ha sparse
Isolated plants
Isolated plants
Pilbara, Western Australia
Mardie Station
21°11:2940 S
115°56:9480 E
‘‘Hybrids’’
30,000 ha dense; 120,000 ha
sparse
Gascoyne, Western Australia
Carnarvon
24°53:8300 S
113°42:3200 E
‘‘Hybrids’’
Isolated plants
McKinlay Township
Longitude
Regions were mostly summer-rainfall, although the
Pilbara can get significant winter rainfall, the Gascoyne
is primarily winter rainfall, and northwest New South
Wales can receive rainfall throughout the year. All regions were semiarid to arid (average of 230–521 mm
annual rainfall) (Fig. 2B). Rainfall typically varies
greatly from year to year within these regions, so longterm averages do not necessarily represent year-to-year
rainfall. For example, annual rainfall has varied from 9
to 856 mm in the Pilbara region (Mardie Station) in the
past 100 years. Nonetheless, average rainfall in the native range encompassed most Australian average rainfall
patterns, except the winter rainfall in the Gascoyne and
Pilbara regions (Fig. 2B).
2.3. Mass-rearing and release methods
Both insects were mass-reared in the laboratory on
whole potted plants. The release strategy was to make
multiple releases of relatively large numbers of insects at
a few sites within each region.
2.3.1. Evippe
The mass-rearing culture was established from 286
adults which emerged from leaf-ties taken from five
Prosopis vinalillo Stuckert trees at a single site in
northern Argentina (Santiago del Estero Province,
18 km NE A~
natuya, 28.08°S, 62.44°W, 108 m a.s.l.) in
December 1997. Genetic diversity was maximized in the
initial generation by setting up cages with 10 pairs of
Isolated plants
adults each (0–3 pairs from each tree). Breeding adults
were pooled randomly in subsequent populations.
Evippe was mass-reared by placing 40–200 adults in
gauze cages together with three to six potted plants
(150 mm diameter pots or equivalent) (P. velutina, P.
pallida, P. glandulosa, P. juliflora (Sw.) DC., and/or
hybrid Prosopis). More plants were added as required.
From June 1998, cultures were kept under grow lamps
(ca. 16 h per day) during the winter moths (mostly at
23 °C or higher) to prevent initiation of diapause. Evippe
were mostly shipped as late-instar larvae because adults
are relatively fragile and most eggs are oviposited within
the first week. Excess adults were also shipped when
available, in 250 or 500 ml clear plastic containers lined
with blotting paper, holding 50 and 100 adults, respectively. Culture plants were cut down when most immatures were at or near the pupal stage and the foliage
freighted to their release destinations in polystyrene
boxes. Estimates of release sizes were based on 100 immatures per plant in a 150 mm-diam. pot, and 150 immatures per plant in a 200 mm-diam. pot, or a
percentage thereof if less than 100% of foliage was attacked. These are conservative estimates based on several months of culturing data.
Boxes with leaf-ties were placed directly into the field,
generally within 48 h of harvesting. They were tied to
mesquite trees and holes cut in them to allow adults to
emerge. Adults were released without constraint. Fieldcollected leaf-ties were redistributed from some sites:
within Mardie (November 1999), from Mardie to P.
12
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
Fig. 2. Average monthly temperatures (A) and rainfall (B) at the point of origin of both agents and the six regions in Australia where releases were
made. Data were obtained from the closest meteorological station to the main infestations at which most releases were made. Native range temperatures (Aimogasta to Santiago del Estero) and rainfall (Aimogasta to Anatuya) give the full range of conditions across collection sites.
pallida infestations on Minderoo Station (near Onslow,
November 1999), from the Hughenden release site to
other sites within the Hughenden region (July–August
1999), and from Alroy Downs to Alexandria, Rockhampton Downs (August 1999), and Lake Nash (October 1999). No follow-up surveys were made at
Minderoo Station (Pilbara Region), Alexandria, or
Rockhampton Downs (Barkly Tablelands).
2.3.2. Prosopidopsylla flava
The culture originated from more than 330 adults
collected from P. chilensis (Molina) Stuntz in northern
Argentina in April 1997 (La Rioja Province, Rt. 9,
56 km N La Rioja city, 28.45°S, 66.38°W, 640 m a.s.l.)
and November 1997 (about 73 km to the north, La
Rioja Prov., 2 km SW Aimogasta, 27.47°S, 64.15°W,
853 m a.s.l.). Large cultures were maintained in quarantine for host-specificity testing for 18 months (van
Klinken, 2000). A total of 14,220 adults were subsequently removed from quarantine over a two-month
period to establish cultures for mass-rearing.
Mass-rearing was done as for Evippe, with 300–400
adults placed into each cage. All mass-rearing during the
cooler months was done under grow lamps (mostly at
23 °C or higher). P. flava proved difficult to transport
because both immatures and adults die quickly in the
absence of their host plant and are sensitive to hot, dry
conditions. The most efficient shipping method with the
highest survival was found to be as adults held on
freshly cut foliage in insulated containers lined with
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
absorbent paper. The paper was sufficiently moistened
to prevent the cut foliage from desiccating, yet retain the
capacity to absorb any condensation to which the adults
may stick. Adults were harvested directly into plastic
containers using a hand-held vacuum aspirator. Adults
for release were rarely more than one-week-old as cages
were harvested 1–2 times per week.
Most releases were made within 36 h of harvesting.
The psyllids were released in different ways: free-release
onto trees (1998/99, mostly); free-release onto antproofed trees (1999/00, mostly); and initial release into
gauze sleeves for 2–30 days (if a return visit was possible). Trees were ant-proofed by isolating them from
other vegetation and the ground. Touching vegetation
was pruned away and the trunk wrapped in foam rubber
that was coated in a thick, sticky gel (STIKEM SPECIAL, Seabright Laboratories, Emeryville, California),
which prevents access by crawling insects. Where possible, trees that did not have a resident ant population
were selected.
2.4. Survey methodology
Most release sites were visited one or two times a year
to survey insects. Where possible, visits were conducted
in early summer and just prior to winter. Local, trained
weed officers sometimes made supplementary surveys.
2.4.1. Evippe
Leaf-ties are easily locatable because the senescent
pinnules stand out among the undamaged, green foliage,
even at low densities. All trees within 20 m of the release
point (an arbitrarily determined standard) were walked
around, and the density of leaf-ties recorded on each.
When leaf-ties were uncommon, the total number of
leaf-ties was recorded. At higher densities, counting individual leaf-ties was not possible, so the percent of total
foliage present that was leaf-tied was estimated. Estimates of percent leaf-attack by different observers were
calibrated once or twice a year in each region (by R. van
Klinken), and independent estimates were always within
0–20% of each other. At some sites, transects or spot
checks were done away from the release point to determine spread of Evippe. Leaf-ties reached very high
densities at some sites, so post-release evaluations were
subsequently categorized into six density categories:
from no leaf-ties to an average of 90% or more of foliage
leaf-tied. Density was designated as less than 1% of foliage if leaf-ties could be individually counted.
2.4.2. Prosopidopsylla flava
The following surveying techniques were tried: visual
searching of foliage in situ for eggs, nymphs, and adults;
beating of foliage onto a beating tray; beating of cut
foliage onto a white sheet (ca. 1 1:5 m); and visual
search of plants for distorted foliage caused by nymphal
13
feeding on immature growth. All techniques detected
psyllids at relatively low densities. However, beating of
foliage was impractical under wet or windy conditions,
and visual searching of foliage for psyllid individuals
and use of beating trays were very labor intensive. The
most efficient technique therefore was to search for leafdistortions and to open them up for evidence of psyllid
activity (presence of nymphs and/or nymph frass). This
technique rarely detected nymphs feeding on mature
foliage or stems, though they rarely do this when immature foliage is available. It also rarely detected adults.
Psyllid density was categorized into four categories:
from no psyllids or distorted pinnae per plant to ‘‘some
plants with more than 100 psyllids or distorted pinnae.’’
Dispersal from the release tree was categorized as recorded on the release tree only, within 20 m of the release tree and more than 20 m from the release tree.
2.5. Psyllid sleeve trials
Early post-release surveys found few or no psyllids,
despite large releases at some sites. Psyllids were therefore placed in polyorganza or gauze sleeves at some
sites, which were revisited to determine whether oviposition and development could occur when contained in a
sleeve and in the absence of predators. Sleeves were
further protected against predators (particularly ants)
by isolating branches and applying STIKEM SPECIAL
proximally.
2.6. Climate-matching
The climate between the origin of both agents and
those in rangeland Australia were compared quantitatively using the climate-matching function in CLIMEX
(Sutherst and Maywalk, 1999). This function allows a
quantitative comparison between climate at a single location in the native range, with other locations. Meteorological data (mean monthly minimum and maximum
temperatures and relative humidity, total rainfall, and
rainfall pattern) are compared between sites to generate
a weighted index (Sutherst et al., 1999). We chose Santiago del Estero (27.47°S, 64.15°W, 199 m a.s.l.) to
represent the point of origin of both insects as it was the
closest meteorological station to collection sites that
recorded relative humidities.
3. Results
3.1. Evippe release and post-release data
Almost 62,000 individuals (conservatively estimated)
were released between March 1998 and February 2000,
mostly as either late-instar larvae or pupae (Table 2).
Average release sizes were 1109 (410–2975; n ¼ 44) im-
14
Table 2
Summary of Evippe sp. #1 releases and post-release evaluations at each infestationa
Infestation and release point
Releases
% Immatures
(of total)
No. individuals (no. releases)
1998–99
1999–2000
New South Wales
One Tree
White Leeds
1090 (1)
2180 (1)
2149 (2)
3486 (6)
–
7368 (9)
Queensland (south-west)
Comongin (Lake)
Comongin (Bruchid)
1053 (1)
2107 (1)
3011 (3)
7962 (6)
–
–
Queensland (north)
Hughenden
Hampden Downs (Kennedy Dam)
Hampden Downs (Wild Duck Ck)
McKinlay Township area
Moorooka
–
–
–
–
–
4812
2065
1146
–
625
–
–
558 (1)
670 (1)
–
Barkly Tablelands
Alroy Downs
Austral Downs
Lake Nash
2000 (1)
1000 (1)
1000 (1)
2677 (2)
1520 (2)
1728 (2)
–
–
–
Pilbara
Mardie (Du Boulay)
Mardie (Jillan Jillan)
Mardie (Woolshed)
–
–
–
5555 (3)
1795 (2)
2625 (3)
–
–
–
Gascoyne
Carnarvon
–
1600 (1)
–
65.0
Total
10,430
42,756
8596
79.0
a
(4)
(3)
(2)
(1)
1998–1999
1999–2000
2000–2001
Early
Late
Early
Late
Early
Late
83.8
59.6
–
1
1
1
1
1
1
1
1
1
1
2
87.5
93.0
–
0
1
1
1
1
3
2
–
–
3
3
73.9
61.7
43.1
67.2
100
–
–
–
1
1
1
1
–
–
–
–
–
3/2c
2
1
2
1
1
–
–
–
–
4/2c
–
–
–
–
77.5
71.0
66.8
–
–
–
2
1
1
1
0
1
3
–
All adult plants killed
–
–
–
0
0
1
3
3
4
5
5
4
5
4
4
4
4
4
4
4
4
–
3
–
–
–
–
100
100
100
3
Observations made at least one year after the last release are in bold font.
Leaf-tie densities: 0, no leafties found; 1, <1% of foliage leaf-tied on most plants; 2, 1–10% of foliage leaf-tied on most plants; 3, 10–50% of foliage leaf-tied on most plants; 4, 50–90% of foliage
leaf-tied on most plants; and 5, 90% or more of foliage leaf-tied on most plants.
c
<3 m trees; >3 m trees.
b
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
Mar–Jun 98
Leaf-tie abundanceb
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
matures, and/or 382 (47–1104; n ¼ 34) adults. Immatures always arrived in good condition, but adults are
relatively fragile and short-lived, and only 68% survived
shipment overall. Releases in New South Wales and the
Northern Territory in March–June 1998 were predominantly of diapausing larvae, but remaining releases were
not. Releases were made at 16 sites in 12 infestations.
Multiple releases were made at most sites, with up to 16
releases at any one site (White Leeds, NSW).
Where return visits were made, leaf-ties were present
at all release sites at least one year after the last release
(Table 2). Even single, relatively small releases (Moorooka, McKinlay Township, and Carnarvon) were sufficient to establish breeding populations, although
Carnarvon was only revisited after 4 months and
McKinlay after 1.5 months. Leaf-ties reached very high
densities within the first season at sites in the Pilbara,
where most trees had more than 50%, and frequently up
to 100%, of foliage leaf-tied by the end of 1999. High
levels of attack continued throughout the survey period.
Populations increased more slowly at other sites and
never reached mean densities of 10% at sites in New
South Wales.
With the exception of the Pilbara, leaf-tie densities
were typically very low early in the season and highest
late in the season (Table 2). Leaf-tie densities in infes-
15
tations in north Queensland and the Northern Territory
(all P. pallida) were inversely correlated with tree height.
This was quantified on the Barkly Tablelands (Alroy
Downs, May 2001) where leaf-tie densities on plants up
to 3 m tall (39 5 (SE)%; n ¼ 42) were higher than on
plants taller than 3 m (11 2 (SE)%; n ¼ 21) (t test:
P < 0:01). Plant size and leaf-tie density were not correlated at other sites.
Evippe spread (as indicated by the presence of leafties) was recorded at some sites, but was underestimated
because surveying away from release points was generally not systematic. Also, surveys were generally too
close to release points to record the actual, high rate of
dispersal properly. Within one year of initial releases,
moths had spread at a rate of at least 1.3–3.6 km/year
(Pilbara, three sites), 2.7 km/year (Alroy Downs, Barkly
Tablelands), 3 km/year (Hughenden, north Queensland),
and 1.1 km/year (southwest Queensland). Within two
years, leaf-ties in the Pilbara were found 11 km from the
closest release site (6.9 km/year). Within three years,
leaf-ties were found on an isolated mesquite plant near
Richmond, ca. 115 km from the closest release site in
Hughenden (north Queensland), an average dispersal
rate of 43 km/year (L. Fleck, personal communication,
Queensland Department of Natural Resources and
Mines, Hughenden, Qld).
Table 3
Summary of P. flava psyllid releases and post-release evaluations at each infestationa
Infestation
Abundance and spreadb
Releases
No. of
sites
No. of live individuals
(no. releases)
1998–99
1999–2000
% Survival
1998–1999
1999–2000
2000–2001
Early
Late
New South Wales
One Tree
White Leeds
1
2
5223 (4)
2293 (3)
2956 (1)
24,136 (7)
88.6
93.4
0
0
–
2 1A,
3 2A, 2B
1B
–
0
1B
Queensland (south-west)
Comongin
3
4447 (4)
22,695 (17)
92.4
0
1A, 2A, 2B
1A
2C
Queensland (north)
Hughenden
6
11,818 (6)
26,877 (22)
97.2
1A, 2B
1A
0
Hampden Downs
Moorooka
2
1
3936 (3)
980 (1)
2280 (1)
–
90.1
93.3
0
–
1A
–
2 1A,
1 1B
–
–
–
–
2
1
1
6362 (3)
1950 (2)
1171 (1)
16,740 (4)
–
–
92.9
72.2
97.6
0
–
0
0
0–
–
–
–
0
–
–
Pilbara
Mardie
15
2259 (5)
46,755 (26)
85.1
0
2B
1B, 2A, 2B
0
Total
34
40,439
142,955
90.9
Barkly Tablelands
Alroy Downs
Austral Downs
Lake Nash
a
Observations made at least one year after the last release are in bold font.
b
Density: 0, no psyllids; 1, <10 psyllids and/or distorted pinnae per plant; 2, some plants with 10 to >100 psyllids and/or distorted pinnae; 3, some
plants with >100 psyllids and/or distorted pinnae. Spread: A, release tree only; B, within 20 m of release tree; and C, more than 20 m from release tree.
16
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
3.2. Psyllid release and post-release data
Almost 183,000 live adults (excluding the 9.1% that
died in transit) were released between October 1998 and
June 2000 into 10 infestations (Table 3). However, in
1999–2000 most releases were restricted to one infestation in each of five of the six main climatic regions in
which mesquite infestations occur. No releases were ever
made in the Gascoyne region. Multiple releases were
made at each site, although this was hampered in the
Pilbara because foliage on trees used in earlier releases
were frequently almost completely consumed by Evippe.
Psyllids or psyllid feeding damage, were found at
most infestations during post-release surveys (Table 3).
Densities were always low, with generally less than 10
psyllids or distorted pinnae per tree, and psyllids were
never found far from the original release trees. By late
2000–2001, P. flava was only recorded from two infestations, in New South Wales and southwest Queensland,
despite intensive searches at release sites in other regions
(Table 3).
At Comongin (southwest Queensland), psyllids were
still present at one of the three release points one year
after the last release. At this site, 15,107 adults were
released in 10 releases between January 1999 and May
2000. By April 2001, adults were sparsely distributed up
to 50 m from the original release tree, with a few individual plants having more than 100 distorted pinnae. At
the two failed sites, 4725 adults (in four releases) and
7310 adults (in seven releases) were released respectively.
Psyllids were recovered at both these sites up to
9 months following the most recent releases, but not
after 12 months.
At White Leeds (northwest New South Wales),
psyllids were still present 14 months after the last release.
Psyllids were rare (maximum of 36 distorted pinnae on a
single tree) and only found within 20 m of the original
release tree. At One Tree Station, also in New South
Wales, psyllids were found within 9 months of the last
release, but not after 14 months.
3.3. Pysllid sleeve trial
Adults were released onto sleeved branches on eight
occasions at four infestations (Table 4). Most sleeves
were subsequently checked for eggs. In each case, eggs
were abundant (Table 4), and egg hatch rates (ca. 90%)
were comparable with those recorded in the laboratory
(van Klinken, 2000). Nymphs were abundant in sleeves
set up in the Pilbara (including in mid-winter), but were
uncommon or absent in sleeves in New South Wales,
although sleeves may not have been entirely ant-proof
there (Table 4).
3.4. Climate-matching
Climate-matching using CLIMEX showed a broadly
similar pattern (Table 5) as qualitative comparisons
(Fig. 2). Climates were compared quantitatively between
the native origin (represented by Santiago del Estero)
and Australia for the different climate parameters, both
individually and in combination (Table 5). Relative
Table 4
Observations of P. flava syllids released in sleeves
Infestation
Month (no. sleeves)
Pilbara: Mardie Station
June (6)
October (2)
November (4)
Average no. adults/sleeve
Egg abundance
Days to nymph survey
Nymph abundance
150
Abundant in all
sleeves
Abundant in all
sleeves
Abundant in all
sleeves
30
–
Abundant in all
sleeves
Abundant in all
sleeves
NA
75
100
43
North Queensland: Hughenden
February (1)
300
Abundant
–
NA
Southwest Queensland: Comongin
January (4)
450
Abundant in all
sleeves
Abundant in all
sleeves
Abundant in all
sleeves
–
NA
–
NA
–
NA
26
Uncommon in five
sleeves, absent in the
remainder
February (4)
300
March (3)
600
New South Wales: White Leeds
October (12)
193
NA
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
17
Table 5
Climate matching between the native origin (Santiago del Estero) and Australiaa
Regionb
North-west New South
Wales
South-west Queensland
North Queensland
Barkly Tablelands
Pilbara Region
Gascoyne Region
Individual parametersc
Combined parameters
Tmin
Tmax
RFtot
RFpat
RH
Temperature + RF
Temperature
RF
62
69
64
74
24
55
53
56
85
67
51
53
53
80
62
55
47
47
74
96
84
70
70
86
86
84
74
74
11
18
11
30
30
72
73
61
51
51
75
52
38
35
35
71
86
78
61
61
a
0 (no match) to 100 (identical match). Values above 70 are in bold.
Data was used from the meteorological station that was closest to each main release infestation: Broken Hill, Quilpie, Hughenden, Brunette
Downs, Port Headland, Carnarvon, respectively.
c
Tmin : Minimum temperature; Tmax : maximum temperature; RFtot : total annual rainfall; RFpat : rainfall pattern; RH : relative humidity (see
Sutherst et al., 1999 for a full explanation of indices).
b
humidity was poorly matched at all sites (Table 5), being
much lower in Australia. When temperature and rainfall
were combined, relatively close matches (>0.7) only
occurred with south-west Queensland and north
Queensland, and only south-west Queensland had closely matched temperature conditions. The worst matches were in the Pilbara and Gascoyne regions in
Western Australia, especially for temperatures.
4. Discussion
Evippe is now widely established in all regions within
Australia where releases have been made, although leaftie abundance differs greatly between regions. The only
places where releases were not made are in arid South
Australia, the Kimberley (northern Western Australia),
and Victoria, all of which have infestations with few
plants (van Klinken and Campbell, 2001). In contrast,
P. flava is only tenuously established at two release sites
in two regions.
4.1. Evippe
Evippe established easily at most sites, including in
very sparse infestations, such as at One Tree Station in
New South Wales (Tables 1 and 2). Even single, relatively small (<1000 individuals) releases were sufficient
for establishment. Moths were good dispersers, and their
populations expanded at least 1 km a year, but probably
much faster as dispersal of up to 43 km per year was
recorded in north Queensland. The moths found even
isolated trees. At Alroy Downs (Barkly Tablelands),
isolated trees, scattered several kilometres out from the
core infestation, were all infested. In north Queensland,
leaf-ties were found 115 km away from the original release site within three years, despite there being relatively
little intervening mesquite. Excellent dispersal ability
means that Evippe can became established even when
mesquite populations are exceedingly sparse, and can
reinvade rapidly after broad scale control using fire,
mechanical, or chemical measures is effected.
The proportion of foliage that is leaf-tied can vary
greatly through the season, depending on the timing,
degree, and synchrony of leaf production and leaf-drop,
as well as moth abundance and activity. Comparisons of
relative leaf-tie abundance data between sites (Table 2)
are therefore limited by the infrequency of visits to most
infestations. Nonetheless, population increases clearly
varied considerably between regions, being fastest in the
Pilbara where populations reached saturation point
within two years, and slowest in northwestern New
South Wales where moth populations were still very low
(<10% foliage is leaf-tied) after three years.
It is yet to be determined what level, timing, and
duration of defoliation is required to cause significant
changes in development rates, survival, and reproduction of mesquite. However, significant impact is expected
in the Pilbara, where leaf attack is very high (mostly
above 50% and frequently above 90%) and prolonged.
Relatively high leaf loss (at least 10–50%) does occur in
other regions (with the exception of northwest New
South Wales), but it appears to take much of summer to
reach these levels, by which time impact might be negligible. Higher early summer populations will probably
be required to cause significant impact at these sites, and
it is yet to be seen whether this will occur. The effect of
winter leaf drop in cooler infestations (van Klinken and
Campbell, 2001) may also limit the increase in moth
numbers early in the season (through increased winter
mortality), but this has not been studied.
Circumstantial evidence from Mardie Station (Pilbara Region) suggests that Evippe densities are independent of mesquite taxa and supports laboratory
studies that show no differences in performance on the
different mesquite taxa in Australia (van Klinken and
Heard, 2000). The hybrid infestation on Mardie Station
has several morphotypes that grow side by side. Parent
18
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
species probably include P. pallida, P. velutina, and P.
glandulosa var. torreyana (van Klinken and Campbell,
2001), and are the same species that are present at the
other release infestations (Table 1). Evippe activity was
uniformly high on all plants on Mardie Station, and
there was no evidence of preference for particular
morphotypes.
Density of Evippe was broadly correlated with mean
temperatures. Both leaf-tie densities and mean temperatures were highest in the Pilbara (>50% of foliage leaftied), the converse was true in northwest New South
Wales (<10%), and both leaf-tie densities and temperatures were intermediate in other regions (Fig. 2). Leaf-tie
densities would be expected to be lower in southwest
Queensland than in northern Australia, but this was not
apparent with the available data. Temperatures were on
average 4.7 °C hotter in the Pilbara than in the insectÕs
point of origin. Densities of Evippe showed no obvious
relationship with rainfall pattern. For example, Pilbara
and northwest New South Wales were two of the drier
sites (Fig. 2), but had very high and low leaf-tie densities
respectively (Table 2). Similarly with climate-matching
using CLIMEX, Evippe performance bore little or no
relationship with climate-matching scores, doing best
where the match was worst (Table 5). Climatic conditions in the point of origin are therefore a poor predictor
of Evippe performance in Australia.
might be best there, and that hot conditions might be
important in limiting psyllid populations. These regions
have similar temperatures and rainfall to the native
range (Fig. 2). Climate-matching predicted the relatively
good performance in south-west Queensland (if relative
humidity is excluded), but not in northwest New Wales.
The poor match in relative humidity throughout Australia, might also play a factor, although microclimate
may have a moderating influence.
Strong circumstantial evidence suggests that ants are
also likely to be an important factor in preventing establishment and limiting populations. Ants were generally abundant at all release sites, and nymphs are
free-living and exude no excretions that might limit
predation (van Klinken, 2000). Nymphs can live between the appressed pinnules of distorted growing tips
that result from nymphal feeding (which would also
serve to provide a more humid microclimate). The
dorsoventrally flattened bodies fringed with hairs may
assist in this cryptic behavior, but this appears not to be
sufficient to prevent predation by ants. Any competitive
interactions with Evippe is probably limited to the Pilbara, where most or all foliage was frequently consumed, including on release trees.
4.2. Prosopidopsylla flava
The two new biological control agents of mesquite
perform differently across Australia despite coming
from the same region in Argentina. Evippe reached
highest densities in the Pilbara where conditions contrasted most strongly with those at the point of origin.
In contrast, the psyllid only established at sites where
the climate was most similar to the native range, although other factors affecting establishment success,
such as predation by ants and competition from Evippe
(in the Pilbara), cannot be ruled out. Climatic similarity
with the native range was therefore a poor predictor of
establishment and relative performance, at least for
Evippe. Ecoclimatic matching can therefore be misleading because it does not account for specific climatic
parameters that are most important in determining
abundance of the insect in question. It was certainly not
sufficient at the resolution required to predict comparative performance under different climatic conditions
within Australia.
Additional biological control agents are almost certainly required, especially in eastern Australia where
mesquite infestations are large and the existing agents
will probably exert insufficient control on their own.
There is certainly a large pool of potential biological
control agents available, with over 945 phytophagous
insect species having been recorded on mesquite in the
Americas (van Klinken and Campbell, 2001). New
agents will either need to have wide climatic tolerances
Prosopidopsylla flava failed to establish at most sites
despite large release sizes and despite being released on
multiple occasions at some sites. For example, 11,690
live adults were released over four occasions at one release point in the Pilbara yet these failed to establish.
Poor establishment rate was not due to problems in
shipment methods because adults were healthy and fecund on arrival (Table 4). At the two sites where P. flava
has established, population densities are very low and
dispersal appears to be slow (although dispersal rates
are difficult to determine when population densities are
low). P. flava is therefore tenuously established and is
currently having no impact on mesquite populations.
Possible explanations for failure to establish and/or
reach damaging densities include climatic factors, predation, host quality (Hodkinson, 1974), competition
with Evippe, and inbreeding in laboratory cultures.
Psyllids were in culture for 18–38 months (11–23 generations at 50 days/generation) prior to release so inbreeding cannot be ruled out, although psyllid numbers
remained large throughout. Sleeve trials in each region
confirmed that nymphal development occurred under
field conditions, at least in the Pilbara and northwest
New South Wales. Nonetheless, the fact that P. flava
only established in southwest Queensland and northwest
New South Wales suggests that climatic conditions
5. Conclusions
R.D. van Klinken et al. / Biological Control 26 (2003) 8–20
to perform well throughout the mesquite distribution in
Australia (Fig. 2), or agents will be required to target
specified climatic regions (e.g., north and southwest
Queensland).
Climate-matching is clearly inadequate for predicting
which potential agents will perform best under particular climatic conditions in Australia, and climate-modeling, which takes into account the requirements of
individual insects or pathogens, is therefore required.
Some analytical tools are already available, including
day–degree models and CLIMEX, but the data required
to make sufficiently accurate predictions often is not.
One valuable data source is a detailed understanding of
the native-range distribution of each potential agent,
which can in turn be used to infer physiological parameters through iteration (Julien et al., 1995; Sutherst
et al., 1999). Even better resolution can potentially be
obtained from quantitative field data on abundances
and phenology (Scott, 1992). However, not all climatic
combinations may be represented within the native
range. For example, nowhere in the Neotropics is as
uniformly hot as the Pilbara. Describing physiological
requirements in laboratory trials may therefore also be
required, including the effects of temperature and
moisture on development and mortality. The challenge
therefore remains to determine whether improved climate-modeling will lead to a significant improvement in
our ability to select effective agents, and whether it can
be done cost-effectively.
Acknowledgments
We thank Areli Mira, Dalio Mira, and Sounthi Subaaharan for assistance with mass-rearing and shipment
preparation; Rob Cobon, Lyle Fleck, Nathan March
(QDNRM), Drewe Gracie, John McMahon (NT
DPIE), Rob Parr (Western Australia in Department of
Agriculture), and Eric McCormick (NSW Land and
Water) for assistance with releases and field observations; and David Briese and Tim Heard for comments
on the manuscript.
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