Predation and Climate Limit Establishment Success of the Kyushu Strain of the Biological Control Agent Aphalara itadori (Hemiptera: Aphalaridae) ...
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Environmental Entomology, XX(XX), 2022, 1–12
https://doi.org/10.1093/ee/nvac031
Research
Biological Control - Weeds
Predation and Climate Limit Establishment Success of the
Kyushu Strain of the Biological Control Agent Aphalara
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itadori (Hemiptera: Aphalaridae) in the Northeastern
United States
Jeremy C. Andersen1, and Joseph S. Elkinton
Department of Environmental Conservation, University of Massachusetts, Amherst, MA, USA 1Corresponding author, e-mail:
jcandersen@umass.edu
Subject Editor: Michelle Rafter
Received 4 January 2022; Editorial decision 23 March 2022.
Abstract
Species of knotweeds, Reynoutria spp. Houtt. (Caryophyllales: Polygonaceae), including Japanese knotweed
(R. japonica Houtt.), are among the most invasive and ecologically destructive plant species introduced to
North America and Europe. The Kyushu strain of the psyllid Aphalara itadori Shinji (Hemiptera: Aphalaridae)
has been approved as a biological control agent for release against Japanese knotweed in the United
Kingdom, Canada, and the United States. However, recent reports from Canada suggest that both biotic
and abiotic factors may limit its establishment. Therefore, we examined the potential role of predation by
comparing open- versus closed-sleeve treatments, and climate mis-matches by collecting temperature
data from release sites and performing climate suitability analyses using MaxEnt. Our results indicated
that populations of the Kyushu strain could only be maintained in the field in closed-sleeve treatments,
suggesting that predation is likely limiting the establishment success of this strain. In addition, we noted that
daily maximum temperatures at our field sites might exceed documented developmental thresholds for this
strain, and that MaxEnt species distribution modeling indicates no climate similarities between locations in
eastern North America and Kyushu. Combined with previous results, our study suggests that the establish-
ment of the Kyushu strain of A. itadori as a biological control agent for Japanese knotweed may be limited
in eastern North America. We suggest that one strategy to increase the probability of establishment of the
Kyushu strain could be to increase the number of release sites in an effort to find a more optimal niche with
predator-free space.
Key words: knotweed, classical biological control, invasive species, psyllid
The movement of invasive species into new areas has the potential for mechanical, cultural, or chemical controls can sometimes be used to
devastating consequences for naïve ecosystems (Mack et al. 2000). eradicate invasive populations before they spread, become widely es-
While future invasions are unfortunately likely due to human travel and tablished, and have profound economic and ecosystem impacts (Grice
trade (Maxwell et al. 2014), proactive management of invasive species 2009). However, for invasive species with large distributions in an
can mitigate ecosystem impacts, and result in economic savings (Hanley invaded area, the introduction of natural enemies (i.e., classical biolog-
and Roberts 2019). The cost of controlling an invasive species, however, ical control) is often the safest and most cost-effective approach (Van
increases dramatically given both the amount of time since the introduc- Driesche et al. 2010, Van Driesche 2012). This approach works to re-
tion and the geographic area that the invasive species occupies (DOPI unite the invader with one or more of its host specific natural enemies
2010). For recent invaders with limited distributions, combinations of (most frequently an insect or pathogen) from the invader’s region of
© The Author(s) 2022. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: 1
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2 Environmental Entomology, 2022, Vol. XX, No. XX
origin. If these natural enemies establish, the resulting predation/her- Recent studies, aimed at identifying factors that might influence
bivory/disease can potentially reduce the abundance of the invasive the establishment success of the Kyushu strain in Canada, however,
organism to a level that makes it either no longer an economic or en- have highlighted that both biotic factors such as predation and fo-
vironmental pest, or at least a less potent one (Cock et al. 2015, Kenis liage age (Jones et al. 2020) as well as abiotic factors such as hu-
et al. 2017). While concerns exist about nontarget effects following the midity and temperature (Fung et al. 2020) could potentially limit
introduction of natural enemies, studies have shown that these negative its establishment success. Therefore, we compared establishment
consequences are extremely rare in contemporary classical biological success of this strain at field sites in western Massachusetts using
control programs due to the extensive preintroduction testing required open- and closed-sleeve treatments in which we directly documented
in most countries (Cock et al. 2015, Van Driesche and Hoddle 2016, the presence of eggs and early instars, and quantified the number of
Kenis et al. 2017), and that the rates of nontarget attacks have decreased late instar and adult A. itadori, in an effort to measure the poten-
substantially through time as a result of this increased scrutiny (Hinz et tial role of predation in this system. As we did not directly measure
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al. 2019). As a result, biological control is increasingly being integrated predation, nor did we document the presence of predators during
into conservation practices as a response to invasive plants and insects our study, our results will only be suggestive in that predation could
(Van Driesche et al. 2016). cause any differences in abundance between the open- and closed-
Knotweeds, Reynoutria spp. Houtt. (Caryophyllales: sleeve treatments. However, this type of ‘predator-exclusion’ is a
Polygonaceae), are among the 100 most damaging invasive species common study design, and despite these limitations, we are confident
in the world (IUCN 2021), and while native to East Asia (Barney that it will provide at least a preliminary indication of whether or
2006), they have become widely established in many countries not predation might be impacting this system. We also documented
due to their use as ornamental plants. In their invaded ranges, these same life stage parameters in large field cages (2 m × 2 m × 4m)
knotweeds have been shown to reduce the abundance and species that are more similar to ‘natural’ field conditions, but have predators
diversity of vertebrates (Maerz et al. 2005), invertebrates (Gerber present while preventing dispersal. In addition, to better understand
et al. 2008), plants (Murrell et al. 2011), and fungi (Claeson et al. what abiotic factors might limit the establishment of the Kyushu
2014). Chemical and mechanical controls can be partially effec- strain of A. itadori in our region, we compared temperature data
tive in the management of small knotweed stands (Beerling 1990, from our field sites to published ecological thresholds (Myint et al.
Siemens and Blossey 2007), however; in some parts of the world 2012) and performed climate suitability analyses based on public
knotweed species may have been introduced 200 years ago (Conolly records of Japanese knotweed in North America to 1) identify the
1977) and have subsequently spread over vast areas, making this abiotic factors that constrain the distribution of A. itadori in North
type of control both costly and impractical. As a result, extensive America, and 2) to compare how well the climate in North America
effort has been put into identifying suitable biological control agents matches locations in Japan where candidate strains have been col-
for invasive knotweed species (Wang et al. 2008, Kurose et al. 2009a, lected. Finally, we comment on approaches that we believe might
b, Shaw et al. 2009, Wang et al. 2010, Tsuchiya et al. 2011). While improve the establishment success of A. itadori in field settings in the
various pathogens (Kurose et al. 2009a, b, c) and insects (Wang et northeastern United States and elsewhere.
al. 2008, Shaw et al. 2009, Wang et al. 2010) have been observed
attacking knotweeds, only one agent, the psyllid Aphalara itadori
Shinji (Hemiptera: Aphalaridae), has so far been approved for re- Methods and Materials
lease in Europe and North America (Shaw et al. 2011, Fung et al. Kyushu Strain Colony Establishment
2020, Jones et al. 2020).
On 23-IV-2020, approximately 500 adults from the Kyushu strain
A. itadori is a small plant-sucking insect that is native to East
of A. itadori were delivered from the Oregon State Insectary to the
Asia, particularly from the Japanese archipelago and the Korean
greenhouses at the University of Massachusetts Amherst, where the
peninsula (Burckhardt and Lauterer 1997). This species has only
psyllids were allowed to settle on potted Japanese knotweed plants
been recorded feeding on species of knotweed (Grevstad et al.
(4.5 L plastic buckets) placed inside 61 cm × 61 cm BugDorms
2013), and laboratory experiments found that while egg laying
(BioQuip Products, Rancho Dominguez, CA), and maintained under
occurred on some nontarget species, development was confined
ambient light conditions with a minimum temperature of ~15°C.
exclusively to knotweeds (Shaw et al. 2009). In prerelease lab-
Due to concerns about releasing the psyllids prior to the last frost
oratory studies, A. itadori was observed to cause reductions in
day (typically around 1-VI in western Massachusetts), the adults
plant biomass (Grevstad et al. 2013), and to be extremely host
were then allowed to lay eggs within the BugDorms, and the subse-
specific (Shaw et al. 2009, Tsuchiya et al. 2011). Currently, two
quent F1 generation individuals were used during releases.
strains of A. itadori, which can be distinguished genetically
(Andersen et al. 2016), have been approved for release in the
United States, with releases made or being planned in Washington Predator Exclusion Experiment
State, Oregon, Massachusetts, Rhode Island, and New York. One By 18-VI-2020, sufficient F1 adults had emerged to allow for groups
of these strains, the Kyushu strain, was established from field col- of 20 adults each to be placed into forty 0.5 m × 1 m nylon mesh
lected adults found during surveys in Kumamoto Prefecture in (0.2 mm2 opening size) bags constructed from ‘noseeum fabric’
2004, and maintained in lab colonies since (Shaw et al. 2009). (Online Fabric Store, Greenfield, MA). The bags were sewn shut
The Kyushu strain feeds preferentially on Japanese knotweed, on three sides, and sealed at the bottom by zip-tying the bag to
R. japonica Houtt., and the hybrid Bohemian knotweed, R. x Japanese knotweed stems, and were deployed at four sites on the
bohemica (Chrtek & Chrtková) J.P. Bailey. In the northeastern University of Massachusetts campus (42.39346, −72.535; 42.39625,
United States, Japanese, Bohemian, and Giant knotweed, R. −72.53291; 42.40021, −72.52598; 42.39372, −72.51649), and one
sachalinensis (F. Schmidt) Nakai, may all be present, though site on the Amherst College campus (42.37408, −72.51336). At each
Japanese and Bohemian knotweeds are the most common in this site, half of the bags were haphazardly assigned to the open-sleeve
region (USDA PLANTS Database https://plants.sc.egov.usda.gov/ treatment, which were opened two weeks after the addition of the
home), with the former being most abundant. psyllids to allow for dispersal and/or access by potential predators.Environmental Entomology, 2022, Vol. XX, No. XX 3
The remaining twenty bags were assigned to the closed-sleeve treat- A. itadori in North America, we use public records accessed from
ment and remained sealed throughout the study (i.e., the predator the Global Biodiversity Information Facility (GBIF) database https://
exclusion treatment). Each week, the presence and absence of eggs www.gbif.org (accessed on October 19th 2021) for Japanese knot-
and 1st through 3rd instar individuals, along with the numbers of weed from this region, and performed climate suitability analyses in
4th instars, 5th instars, and adults were recorded. At one of our sites, MaxEnt v. 3.3.3e (Phillips et al. 2006, Phillips and Dudik 2008). Here
two bags (one each of the open- and the closed-sleeve treatments) we use records for Japanese knotweed as a proxy for A. itadori as
were destroyed by a lawn-mower between 23-VII-2020 and 30-VII- there are no public records of A. itadori in the GBIF database, and the
2020. Differences between treatments in the presence/absence of distribution of hosts has been used as a proxy in other host-obligate
both eggs and early instar nymphs were determined weekly based systems (e.g., Johnson et al. 2019, Dang et al. 2021, Schneider et al.
on χ2 tests, and differences in the numbers of 4th and 5th instars and 2022). To reduce sampling biases, we followed recommendations
adults were determined weekly based on analysis of variance tests; presented in (Hijmans and Elith 2021). Specifically, we used the R
Downloaded from https://academic.oup.com/ee/advance-article/doi/10.1093/ee/nvac031/6584711 by guest on 09 June 2022
both sets of tests were conducted in R v. 4.0.2 (R Core Team 2020). package ‘raster’ to create 1 min × 1 min grid cells that covered the
extent of sampled points, and then randomly retained one sample per
Field Cage Releases grid cell for further analyses using the R package ‘dismo’. A second
Large outdoor rearing cages (2 m × 2 m × 4 m; BioQuip Products) were dataset was then subset that only included records east of the Rocky
constructed and placed over field populations of Japanese knotweed Mountain foothills (98° West), to compare conditions specific to the
plants at three of the study sites on 2020-VI-18. While not directly eastern United States. Each dataset was then used to estimate cli-
measured, most plants were estimated to be between 1 and 2 m in mate suitability in MaxEnt independently in comparison to the bi-
height at time of construction. We assume that potential predators were oclimatic variables provided in the WorldClim v.2.1 dataset (https://
present within these cages at the time of deployment as well, and the www.worldclim.org) downloaded with 5-minute resolution, with
cages were open on the bottom to allow access from ground predators Jack-knife analyses performed to measure variable importance. The
but covered with mesh on all four walls and the roof to limit psyllid resulting climate envelope from each dataset was used to predict cli-
dispersal. Into each cage, potted knotweed plants that contained a total mate suitability in both the invasive regions of Japanese knotweed in
of approximately 1,000 A. itadori individuals (all life stages were in- North America, and to the native distribution in Japan and East Asia.
cluded in this estimate), were placed into each cage. The presence of
eggs and early instar individuals, as well as the numbers of late instar
and adults were then monitored and analyzed as described above, ex-
Results
cept that surveys occurred on 10 knotweed shoots chosen haphazardly Kyushu Strain Colony Establishment and Predator
in each cage on each survey date, and our first survey occurred two Exclusion Results
weeks post-introduction. Post-hoc comparisons were performed using Individual adults of the Kyushu strain were observed to settle readily
Tukey’s Honestly Significant Difference test as implemented in R. upon the potted knotweed plants in the University of Massachusetts
Amherst greenhouse. During the first two weeks after release, there
Temperature Data were no significant differences in the presence of eggs (Fig. 1) or of
Previous work on the Kyushu strain of A. itadori has shown that early instars (Fig. 2) between the open- and closed-sleeve treatments.
the proportion of individuals surviving to adulthood is directly de- However, after 2-VII-2020, when the zip-ties were removed from the
pendent on temperature, with maximum survivorship occurring at open-sleeve treatments, there were significant differences between
20°C and decreasing at both lower and higher temperatures, with the treatments (χ2 > 4.8, df = 1, P < 0.05) observed in regards to the pres-
lowest observed survivorship occurring at 30°C (Myint et al. 2012). ence and absence of eggs during three of the eight weekly surveys. For
Being that summer temperatures are frequently at or above 30°C the early instars, these differences were only significant during the 1st
in eastern North America, we obtained maximum (tmax) and min- week immediately following the sleeves being opened (9-VII-2020;
imum (tmin) temperatures (°C) for each of our study sites using the χ2 = 4.61, df = 1, P = 0.032; Fig. 2). No significant differences were
‘Single Pixel Extraction Tool’ at https://daymet.ornl.gov/single-pixel/ observed in the numbers of 4th instars at any point during our survey,
and calculated smoothed conditional means for both tmax and tmin though the mean number of 4th instars never exceeded one individual
values for each day during our survey period using the ‘loess’ function per sleeve (Supp Fig. A1 [online only]). In contrast, there were signif-
implemented in the R package ‘ggplot2’ (Wickham 2009). icant differences (F > 6.38, df = 1, P < 0.05) in the numbers of 5th
instar individuals during five of the eight survey weeks (Fig. 3). From
25-VI-2020 through 23-VII-2020, densities of 5th instar individuals
Climate Suitability Analyses
remained near zero in both treatments, but after 23-VII-2020, the num-
Climate suitability analyses are increasingly becoming an important
bers of 5th instar individuals per sleeve increased in the closed-sleeve
component of biological control agent discovery efforts and pre-
treatment bags and remained constant near two individuals per sleeve.
release testing (Mukherjee et al. 2011, Myint et al. 2012, Olfert et
Significant differences (F > 5.68, df = 1, P < 0.05) in the numbers of
al. 2016, Pratt et al. 2019). For estimating the climate suitability of
adults were seen during all but one of the survey weeks following the
introduced species into novel ecosystems, it is generally preferred to
removal of the zip-ties from the open-sleeve treatment (Fig. 4). Similar
use records from their native distributions when conducting these
to the results for the 5th instars, adult densities remained constant after
analyses, as records from the introduced region are likely to repre-
23-VII-2020 at or near four individuals per sleeve in the closed-sleeve
sent only a fraction of the potential niche into which the introduced
treatments, and no adults were observed in any of the open sleeves fol-
species will eventually occupy (Elith et al. 2011, Merow et al. 2013).
lowing 30-VII-2020.
However, for species such as Japanese knotweed that have existed
in their introduced regions for centuries, these species likely exist
at range equilibrium (Merow et al. 2013), and records from the Field Cage Releases
introduced population are increasingly being used for invasive spe- No eggs or early instars were observed on any of the haphazardly
cies distribution analyses (Barbet-Massin et al. 2018). To better un- selected shoots in the large field cages at any time during the study
derstand which abiotic factors might constrain the distribution of period, even though ~1,000 individuals were introduced to each4 Environmental Entomology, 2022, Vol. XX, No. XX
Presence/Absence of Eggs
P = NS P = NS P = 0.028 P = NS P = NS P = 0.064 P = 0.015 P = 0.015 P = 0.064 P = NS
20
15
Number of Bags with Eggs Present
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10
5
0
C O C O C O C O C O C O C O C O C O C O
25-VI-2020 2-VII-2020 9-VII-2020 16-VII-2020 23-VII-2020 30-VII-2020 6-VIII-2020 13-VIII-2020 20-VIII-2020 28-VIII-2020
Date
Fig. 1. Comparisons of the presence (grey) versus absence (white) of eggs in the closed (left) versus open (right) sleeve treatments (noted with a ‘C’ or an ‘O’,
respectively) for each survey week. The vertical dark line between 2-VII-2020 and 9-VII-2020 represents the point at which the zip ties that sealed the open sleeve
treatment bags were removed. Statistical differences based on χ2 tests between the two treatments are presented above each pair.
Presence/Absence of Early Instars
P = NS P = NS P = 0.032 P = NS P = NS
20
P = NS P = NS P = 0.064 P = NS P = NS
15
Number of Bags with Early Instars Present
10
5
0
C O C O C O C O C O C O C O C O C O C O
25-VI-2020 2-VII-2020 9-VII-2020 16-VII-2020 23-VII-2020 30-VII-2020 6-VIII-2020 13-VIII-2020 20-VIII-2020 28-VIII-2020
Date
Fig. 2. Comparisons of the presence (grey) versus absence (white) of early (1st–3rd) instars in the closed (left) versus open (right) sleeve treatments for each
survey week as per Fig. 1.
cage. On one instance each, a 4th instar individual and a 5th in- period, with most of these having a single adult present (n = 11),
star individual were detected on a haphazardly selected plant. Adults three having two adults present, and one having three adults present.
were detected on 15 of the 260 plants sampled during our study There was a significant difference (F = 5.67, df = 8, P < 0.001) inEnvironmental Entomology, 2022, Vol. XX, No. XX 5
Open Versus Closed Sleeve Treatments − 5th Instars
P = 0.009
P = 0.011
P = 0.005
3
P = 0.006
P = 0.016
Number of Psyllids
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2
1
P = NS
P = NS
P = NS
P = NS
NA
0
C O C O C O C O C O C O C O C O C O C O
25-VI-2020 2-VII-2020 9-VII-2020 16-VII-2020 23-VII-2020 30-VII-2020 6-VIII-2020 13-VIII-2020 20-VIII-2020 28-VIII-2020
Date
Fig. 3. The mean number of 5th instars present in the closed (white) and open (grey) sleeve treatments (noted with a ‘C’ or an ‘O’, respectively) for each survey
week. The vertical dark line between 2-VII-2020 and 9-VII-2020 represents the point at which the zip ties that sealed the open sleeve treatment bags were
removed. Statistical differences based on analysis of variance tests between the two treatments are presented above each pair, and whisker bars representing
the standard error (SE) are shown for treatment.
the numbers of adults present across the survey weeks (Fig. 5), with being the most important variable in both analyses, and Bio1
the 2-VII-2020 survey being significantly different from all other (Annual Mean Temperature) also contributing to the analyses of both
survey weeks based on Tukey’s Honestly Significant Difference test datasets. The full North American analyses also included variables
(adjusted P = 0.011). After 8-VIII-2020, no adults were observed in for the coldest quarter (Bio11—Mean Temperature of the Coldest
any of the field cages. Quarter, and Bio19—Precipitation of the Coldest Quarter), while the
eastern North American analyses included temperature seasonality
(Bio4) and precipitation of the warmest quarter (Bio18).
Temperature Data
Predictions of habitat suitability in North America, showed a strong
The average maximum temperature (tmax) during our study period
match between the recorded distribution of Japanese knotweed in this
was 29.88°C ± 1.58°C, and the average minimum temperature region and its potential distribution (Fig. 7). Interestingly, the analyses
(tmin) during our study period was 16.91°C ± 0.14°C. The max- based on the eastern North American records showed no suitability
imum observed temperature was 35.25°C during our study period to nearly all of western North America (Fig. 7b), suggesting that the
on 19-VII-2020. The minimum observed temperature was 10.17°C distribution of Japanese knotweed in these two regions is regulated by
observed on 20-VIII-2020. Smoothed conditional means for tmax very different environmental factors. Predictions of habitat suitability
and tmin are presented in Fig. 6. in East Asia, based on the North American records, showed strong
climate suitability across most of Japan, and parts of central China
Climate Suitability Analyses (Fig. 8), though the strength of this match differed between analyses
After filtering to remove duplicates and records with no latitude or with the full North American dataset finding a stronger match to more
longitude information, 13,093 North American records of Japanese of the Japanese island of Honshu (Fig. 8a) than the eastern North
knotweed were obtained from the GBIF database. Random selection American dataset (Fig. 8b). Importantly, neither dataset reconstructed
of one record per grid cell resulted in 418 samples being retained, the Japanese island of Kyushu as suitable habitat.
of which 338 were subset into the eastern North America dataset.
Accuracy of the model fit, as judged using the area under the receiver-
operator curve (AUC) approach (Merow et al. 2013), indicated that Discussion
the full North American dataset had an AUC of 0.961 and the eastern Biological control has the potential to cause a safe and sustainable
North American dataset had an AUC of 0.973. In total, six of the reduction in the abundance and impacts of invasive pests (Murdoch
18 BioClim variables provided ≥10% contribution to at least one of et al. 1985, Julien 1987, DeBach and Rosen 1991, Van Driesche and
the MaxEnt analyses (Table 1), with Bio12 (Annual Precipitation) Bellows 1996, Gurr and Wratten 2000, Hoddle 2003, Bale et al.6 Environmental Entomology, 2022, Vol. XX, No. XX
Open Versus Closed Sleeve Treatments - Adults
P = 0.011
8
P = 0.02
6
P = 0.061
Number of Psyllids
P = 0.004
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P = 0.005
P = NS
4
P = NS
P < 0.001
P = 0.002
2
P = 0.001
0
C O C O C O C O C O C O C O C O C O C O
25-VI-2020 2-VII-2020 9-VII-2020 16-VII-2020 23-VII-2020 30-VII-2020 6-VIII-2020 13-VIII-2020 20-VIII-2020 28-VIII-2020
Date
Fig. 4. The mean number of adults present in the closed (white) and open (grey) sleeve treatments for each survey week as per Fig. 3.
Field Cage Releases − Adults
A
0.6
Number of Psyllids
0.4
B
0.2
B
B B
B B B B
0.0
2-VII-2020 9-VII-2020 16-VII-2020 23-VII-2020 30-VII-2020 6-VIII-2020 13-VIII-2020 20-VIII-2020 28-VIII-2020
Date
Fig. 5. The mean number of adults counted on 10 randomly selected knotweed shoots in each of the three field cages for each survey week. Statistical differences
between survey weeks are represented with different letters and are based on analysis of variance tests, with pairwise comparisons based on Tukey’s Honest
Significant Difference test. Whisker bars represent standard error (SE) as per Fig. 3.Environmental Entomology, 2022, Vol. XX, No. XX 7
Aphalara itadori Massachusetts Release Sites
30
Temperature (°C)
25
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20
15
15-VI-2020 1-VII-2020 15-VII-2020 1-VIII-2020 15-VIII-2020
Date
Fig. 6. Smooth conditional means for the maximum (top) and minimum (bottom) temperatures observed at our five field sites in western Massachusetts during
the course of our study.
Table 1. List of BioClim data variables that contributed >10% to either the MaxEnt climate suitability analyses for the Full or the Eastern
datasets
Full dataset Eastern dataset
Variable Percent contribution Permutation importance Percent contribution Permutation importance
Bio12—annual precipitation 23.8 3.2 25.4 30
Bio1—annual mean temperature 21.2 15.1 10.5 8.3
Bio11—mean temperature of the coldest quarter 16.8 0 0 2.8
Bio4—temperature seasonality 1 6.8 12.3 5.6
Bio18—precipitation of the warmest quarter 1.8 1.5 11.6 12.8
Bio19—precipitation of the coldest quarter 10.7 14.7 0 0.3
For each dataset, the percent contribution of each variable, along with its permutation importance based on jackknife analyses, are provided.
2008, Hoddle and Van Driesche 2009, Van Driesche et al. 2010). The Kyushu strain of A. itadori has shown great promise in lab-
For nonnative species, classical biological control programs exploit oratory settings to reduce overall knotweed plant biomass (Grevstad
the coevolutionary relationships between a target pest and a nat- et al. 2013). In our study, from an initial shipment of ~500 adults,
ural enemy from its region of origin, and following the purposeful our greenhouse colonies grew in size easily so that we could place
introduction of one or more natural enemies, preexisting antago- 800 adults into predator exclusion trials, plus an additional ~3,000
nistic relationships may reduce the impact of the invasive organism individuals into field cages, without risk of removal of too many
(Howarth 1991, Murdoch and Briggs 1996, Van Driesche et al. individuals from the colony. Unfortunately, the population growth
2010, Kenis et al. 2017). One of the strengths of classical biolog- that we observed in the greenhouse was in stark contrast to what
ical control is that after a sufficient number of individuals of the we observed in field settings. In both the large field cages (Fig. 5),
natural enemy have been established, their ability to persist across and in our predator exclusion treatments (Figs. 3 and 4), we saw
the landscape results in the sustainable control of the target pest that population sizes either remained constant at levels far below
species (Elkinton et al. 2021). Our results further suggest that estab- the original number of adults introduced or went extinct. A review
lishment of the Kyushu strain of A. itadori in the field may be limited of the classical biological control literature reminds us that the in-
by factors not present in laboratory settings, particularly predation troduction of a candidate natural enemy is by no means a guarantee
and climate-mismatches. As a result, we suggest that a combination of its establishment (Harms et al. 2020), and even if an agent does
of approaches that include increasing the number of sites that the become established, the ability for introduced natural enemies to
Kyushu strain is released at in each region in an effort to find more build the population densities required to reduce the abundance of
compatible niches with enemy-free space (Grevstad et al. 2011) and/ the target pest is often met with 1) genetic incompatibilities between
or perhaps performing multiple introductions at each release site the target pest and the natural enemy, 2) climatic constraints, and 3)
throughout the growing season (van Lenteren et al. 2003) could as- biotic resistance from native predators and pathogens (Goeden and
sist in its establishment. Louda 1976).8 Environmental Entomology, 2022, Vol. XX, No. XX
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Fig. 7. North American climate suitability analyses results based on publicly available records of Japanese knotweed obtained from the GBIF database for all of
North America (top) and only those from eastern North America (bottom) as estimated using MaxEnt. Circles represent Japanese knotweed localities obtained
from GBIF.
We do not believe that the first factor (genotype × genotype experiments have shown that survivorship decreases to only 17.4%
incompatibilities) is restricting field establishment of the Kyushu compared to ~90% at 20°C (Myint et al. 2012). We should note that
strain as the Japanese knotweed plants upon which colonies were it is possible that our open and closed sleeve treatments may have
established in the greenhouse were grown from rhizomes collected modified the microclimate to some regards in one or both of these
at our release sites, and as noted above populations readily estab- factors, and this is something that we hope to examine in future
lished and grew as expected in greenhouse settings. However, it is studies.
important to note that recent work has found that Japanese knot- Another potential abiotic factor that might be limiting the es-
weed genetic diversity may be greater than originally expected in tablishment of A. itadori is photo-period, though this is likely
our region (Tippery et al. 2021). For the second point, however, both more of a problem in southeastern North America compared to
humidity and ambient temperature differences were previously re- the northeastern portion (Grevstad et al. 2022). Our climate suit-
ported to be potential limiting factors for the establishment of A. ability analyses (Figs. 7 and 8), provided further evidence that the
itadori in Canada (Jones et al. 2020). Our temperature analysis indi- Kyushu strain may be poorly suited for establishment in eastern
cated that the maximum temperature at our field sites frequently was North America. Both analyses conducted for the full North
at or above 30°C (Fig. 6), a critical temperature at which laboratory American dataset and the eastern North American dataset, failedEnvironmental Entomology, 2022, Vol. XX, No. XX 9
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Fig. 8. Predicted climate suitability in East Asia, based on analyses of all North American knotweed records obtained from GBIF (top) and only those from eastern
North America (bottom), as estimated using MaxEnt. Kyushu island is highlighted in bold.
to identify any climate match with localities on Kyushu. While pre- either approved or under review for release in the United States. As
vious climate analyses have indicated some degree of suitability such, we recommend that future releases in North America focus on
for the Kyushu strain in eastern North America (Grevstad et al. the approved Hokkaido strain for giant knotweed biological con-
2012), those analyses did find the Kyushu strain to be less suit- trol or the Murakami strain, collected from the Murakami region
able for establishment in the northeastern United States than the of Honshu and currently under review, for Japanese and Bohemian
Hokkadio strain. In addition, we should note that our analyses knotweed.
differ from those presented in Grevstad et al. (2012) in that we used Finally, while we do believe that climate constraints are likely
MaxEnt, compared to Climex, and that we used North American limiting the establishment success of the Kyushu strain, we also want
localities to predict suitable source locations in Japan, compared to emphasize that predation is a potentially important barrier to es-
to Japanese localities to predict suitable establishment locations in tablishment of this strain—and to other strains of A. itadori—in the
North America (Grevstad et al. 2012). Interestingly, our results do northeastern United States. During the course of our study we fre-
find strong matches to other parts of Japan, particularly the main quently observed the presence of black carpenter ants, Camponotus
island of Honshu, and the northern island of Hokkaido—both re- pennsylvanicus (De Geer) (Hymenoptera: Formicidae) at our sites,
gions where additional A. itadori strains have been located and are and ant species were previously suspected to be a limiting factor10 Environmental Entomology, 2022, Vol. XX, No. XX
to A. itadori establishment in Canada as well (Jones et al. 2020). free niches and/or more compatible environments. Finally, while we
However, we should note that similar to Jones et al. (2020) we did did not identify the species of predators that are likely acting as a
not measure predation directly, though on one occasion when we major limiting factor for the establishment, we encourage future
were surveying an open sleeve treatment we did observe predation research focused on documenting their impact on the different life
by C. pennslyvanicus. stages of A itadori.
Caveats
We would like to acknowledge several limitations to our study
Acknowledgments
design. Again, we would like to highlight that we did not directly We would like to thank Jackson Christopher-Callaghan for field as-
record predation, and in fact only observed predation on a single oc- sistance, and Fritzi Grevstad, Rodger Gwiazdowski, Michelle Labbé,
casion (noted above). Therefore, we assume that differences in abun- and Roy Van Driesche as well as Michelle Rafter and two anony-
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dance between the open and closed-sleeve treatments were caused mous reviewers for their comments on an earlier draft of this man-
by predation, however these differences could have also been caused uscript. We would also like to thank Kenneth Lauzier at Amherst
by alterations of micro-climates by the sleeves themselves, and/or College, and the UMass Amherst Grounds Crew for providing study
dispersal. For example, the increased numbers of individuals in the site access.
closed-sleeve treatment environments could signify a more optimal
microhabitat in this treatment compared to the open treatments if
the sleeves themselves regulated humidity and/or temperature to Funding
a more optimal level. Further work is thus needed to determine
This research was funded by a United States Department of Agriculture
if and how the sleeves modify their microhabitats, and how these
Animal and Plant Health Inspection Service (USDA-APHIS) co-
differences influence the development and survival of the Kyushu
operative agreement (USDA-APHIS-10025-PPQFO000-20-0091)
strain. In regards to dispersal, our findings of reduced numbers of
awarded to J.S.E.
adults in open-sleeve treatments compared to close-sleeve treatments
could have been compounded by the dispersal behavior of this life
stage. However, we observed clear differences between open and
Conflict of Interest
close-sleeve treatments for nondispersing life stages as well, and
noted that our field cage population quickly collapsed after its estab- The authors declare no conflicts of interest.
lishment. Combined these suggest that while dispersal may reduce
our overall ability to detect A. itadori individuals in the field, mor-
tality is occurring during nondispersing life stages as well. Supplementary Data
Additionally, we would like to highlight that we observed the Supplementary data are available at Environmental Entomology
presence of three 5th instar individuals during our 2-VII-2020 online.
survey (15 d after deployment). The most rapid published develop-
mental time for a 5th instar A. itadori is 23.4 ± 0.7 days at 25°C
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