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Induction of Cold Hardiness in an Invasive Herbivore: The Case of Hemlock Woolly Adelgid (Hemiptera: Adelgidae)


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As a measure of cold hardiness, we tested the supercooling points or freezing temperatures of individual hemlock woolly adelgids (Adelges tsugae Annand) collected from 15 locations across the north to south range of the adelgid in eastern North America at different times during two winters. Adelgids from the northern interior locations with USDA hardiness zones of 5B-6B had lower supercooling points than adelgids from more southern or more coastal locations (zones 7A and 6B), where minimum winter temperatures were higher. Supercooling points reached a minimum in February in northern but not in southern locations. Laboratory experiments demonstrated that adelgids exposed to colder temperatures (-12 °C) had lower supercooling points after 3 d and adelgids held at 10 °C had higher supercooling points than did adelgids held at 2 °C for the same period. Extending these periods to 7 d produced no further change in supercooling points. Adelgids at northern sites had much lower supercooling points in February 2015 following at least 10 d of much colder weather than adelgids from those same sites in February 2016 following much warmer weather. The induction of cold hardiness produced much year-to-year variation in cold hardiness, especially in northern sites, in addition to concurrently and previously demonstrated genetic differences in cold hardiness between northern and southern adelgid populations. Consequently, the cold temperatures required to kill hemlock woolly adelgids will vary year to year and week to week based on exposure to prior temperatures.
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Physiological Ecology
Induction of Cold Hardiness in an Invasive Herbivore: The
Case of Hemlock Woolly Adelgid (Hemiptera: Adelgidae)
Joseph S. Elkinton,
Jeffrey A. Lombardo,
Artemis D. Roehrig,
Thomas J. McAvoy,
Albert Mayfield,
and Mark Whitmore
Department of Environmental Conservation, University of Massachusetts, Amherst, MA 01003 (;;,
Corresponding author, e-mail:,
Department of Entomology, Virginia Tech, Blacksburg, VA 24061 (,
USDA Forest Service Southern Research
Station, Asheville, NC 28804 (, and
Department of Natural Resources, Cornell University, Ithaca, NY 14853
Subject Editor: Gadi V.P. Reddy
Received 24 July 2016; Editorial decision 4 October 2016
As a measure of cold hardiness, we tested the supercooling points or freezing temperatures of individual hemlock
woolly adelgids (Adelges tsugae Annand) collected from 15 locations across the north to south range of the adelgid
in eastern North America at different times during two winters. Adelgids from the northern interior locations with
USDA hardiness zones of 5B–6B had lower supercooling points than adelgids from more southern or more coastal
locations (zones 7A and 6B), where minimum winter temperatures were higher. Supercooling points reached a min-
imum in February in northern but not in southern locations. Laboratory experiments demonstrated that adelgids
exposed to colder temperatures (12 C) had lower supercooling points after 3 d and adelgids held at 10 Chad
higher supercooling points than did adelgids held at 2C for the same period. Extending these periods to 7 d pro-
duced no further change in supercooling points. Adelgids at northern sites had much lower supercooling points in
February 2015 following at least 10 d of much colder weather than adelgids from those same sites in February 2016
following much warmer weather. The induction of cold hardiness produced much year-to-year variation in cold
hardiness, especially in northern sites, in addition to concurrently and previously demonstrated genetic differences in
cold hardiness between northern and southern adelgid populations. Consequently, the cold temperatures required
to kill hemlock woolly adelgids will vary year to year and week to week based on exposure to prior temperatures.
Key words: supercooling, overwintering mortality, acclimation, invasive species, Tsuga canadensis
Many insects avoid death by freezing in winter by producing cryo-
protectants such as glycerol and other polyols in their hemolymph,
which reduce the temperatures at which they freeze to values well
below 0C(Zachariassen 1985). The temperature at which such in-
sects freeze is known as the supercooling point (Bale 1987,Lee et al.
1987). The production of cryoprotectants is a physiological response
to cold temperatures (Lee et al. 1987). Induction of cold hardiness
due to prior exposure to cold temperatures or acclimation has been
previously demonstrated in a number of insect species (Bale 1987,
Lee et al. 1987). Here we demonstrate it for the first time in the
hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera:
The hemlock woolly adelgid is an invasive forest insect in eastern
North America that was introduced to eastern Virginia prior to
1951 from Japan (Havill et al. 2006). Insects invading a new region
often face climatic conditions that are different from their countries
of origin. That is certainly true of hemlock woolly adelgid, which
originated from near Osaka, Japan, a location that experiences very
mild winter temperatures (Havill et al. 2006). Since its accidental
initial introduction to Virginia, hemlock woolly adelgid populations
have spread south to Georgia and north to upstate New York and
southern parts of Vermont, New Hampshire, and Maine (Orwig
and Foster 1998). Hemlock woolly adelgids are transported by
wind, mammals, birds, and humans (McClure 1990). The adelgid
has caused high mortality of eastern hemlock (Tsuga canadensis
Carrie`re) and Carolina hemlock (T. caroliniana Engelmann) in many
stands throughout the eastern United States (Orwig 2002). Damage
from the adelgid has been most severe in the southern and mid-
Atlantic states, where substantial hemlock decline has occurred in as
little as 4 yr (Eschtruth et al. 2006,Ford et al. 2012). This has caused
major changes in tree species composition in hemlock-dominated
forests (Jenkins et al. 1999,Kizlinski et al. 2002,Orwig et al. 2002,
Stadler et al. 2005,Eschtruth et al. 2006).
Damage from the adelgid has slowed substantially, however, in
its northern range. After 20 yr of adelgid infestation in
Massachusetts, significant hemlock mortality has accumulated
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Environmental Entomology, 2016, 1–7
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much more slowly than in the south (Paradis 2011,Orwig et al.
2012). Colder winter temperatures in the north, which cause greater
overwintering mortality of the adelgid, have been accepted as the
likely explanation for this slow pace of hemlock mortality in north-
ern stands infested with the adelgid (Skinner et al. 2003,Shields and
Cheah 2005,Trotter and Shields 2009). Studies by Skinner et al.
(2003) showed that adelgids collected during winter from southern
states suffered higher mortality when exposed to cold temperatures
than adelgids collected from northern states. A common garden
study by Butin et al. (2005) with adelgids collected from Maryland
(hardiness zone 6B) and from Massachusetts (hardiness zones 5B
and 6A) showed that the adelgids from Maryland had higher cold-
induced mortality than those from Massachusetts after they were
reared together for two generations (one year) at a site in
Massachusetts. These results suggested that the adelgid in northern
locations had evolved some degree of cold hardiness. In other words,
the difference in cold hardiness between northern and southern
populations is at least partially genetic.
Hemlock woolly adelgids feed on the ray parenchyma cells of
hemlock twigs by inserting their stylets at the base of needles (Young
et al. 1995). As the overwintering sistens generation mature in late
fall, they secrete a white, protective wool-like wax, beneath which
they oviposit in late winter (McClure 1989,1991). The eggs hatch in
March, April, or May (depending on latitude and elevation), produc-
ing the springtime progrediens generation (McClure 1989,Joseph
et al. 2011). Some progredientes (plural of progrediens) become
winged sexuparae. In their native Japan, the sexuparae disperse to
spruce (Picea spp.) and initiate a sexually reproducing generation. In
North America, however, none of the offspring of these sexuparae
survives on the native spruce species. Thus, only parthenogenic repro-
duction occurs in North America (McClure 1989). The progrediens
crawlers settle on hemlock shoots produced in the previous yea. They
mature and oviposit in May or June, and eggs hatch in May, June, or
July. The resulting sistens crawlers enter a period of summer aestiv-
ation, where feeding and development cease. Feeding and develop-
ment resume in October, and continue throughout winter. The
adelgids reach maturity in late winter or early spring.
Here we further explore the causes of the differences in cold
hardiness between northern and southern populations of the adelgid
by analyzing the freezing temperatures or supercooling points of
adelgids collected from 15 locations, spanning the range of adelgid
from north to south in the eastern United States at different times
during the winter. We also report the results of laboratory experi-
ments, in which adelgids were exposed to different cold tempera-
tures for 3 and 7 d to assess the degree to which cold hardiness
could be induced by exposure to cold.
Materials and Methods
Adelgid Collection
To determine the variation in cold hardiness across their introduced
range, we tested the supercooling point of hemlock woolly adelgid
from 15 sites spanning northern Georgia to New York and
Massachusetts (Fig. 1;Table 1). Hemlock twigs infested with adelg-
ids were removed from branches within a height of 2 m from hap-
hazardly selected trees at each site. The samples consisted of small
branches (25–35 cm in length) with a moderate–high density of
live, apparently healthy adelgids on branch tips of the most recent
growth. The samples were placed in insulated boxes and transported
by car or via overnight mail to Amherst, MA.
Measuring Supercooling Points
Supercooling tests were conducted within 2 d of sample collection.
Prior to the test, samples were held in a Percival growth chamber
(Perry, IA) at 2C. The samples consisted of small branches (25–35 cm
in length) with a moderate–high density of live, apparently healthy
adelgids on branch tips of the most recent growth. To measure its
supercooling point, an individual adelgid was selected from a sample
branch, the waxy outer covering (“wool”) was removed with fine-
tipped forceps, and the individual was attached to the end of a K-type
thermocouple sensor using clear tape. The thermocouples were placed
into a container containing small brass beads to facilitate heat conduc-
tion. The container was submerged in a supercooling bath (Neslab
RTE-140) and the temperature of the bath was slowly reduced from a
change every 5 min). The temperature of each adelgid was recorded in
1-s intervals using a multichannel thermocouple recorder (Physitemp
Inc., NJ). The point at which the adelgid froze produced an obvious
spike in the temperature as a result of the heat of fusion. We used the
temperature in the second before the thermal spike as the supercooling
point. The supercooling points of 20–50 adelgids per site per sampling
event were measured. Twenty adelgids per site were sufficient to esti-
mate the trends we were seeking to demonstrate, but we did more of
them whenever time and the number of adelgids available on our sam-
ple twigs permitted. These sites were sampled in February, March, and
December 2015, and in February 2016, but we were not able to collect
from every site in each of the 4mo. A list of sites used in the four sam-
pling events can be found in Table 1.
Differences in the supercooling point of adelgid among the various
source populations were analyzed using regression of supercooling
points against the mean minimum winter temperature (coldest day of
the year) experienced at each collection site over the past 10 yr
(2006–2015). Daily temperature data were obtained from the nearest
NOAA weather station to each site. Regression analyses were con-
ducted in R (RCoreTeam2015). Differences in supercooling points
between months at each site were analyzed by ANOVA coupled with
Tukey’s HSD test SAS (Proc GLM, SAS 9.3, SAS Institute 2012).
Induction of Cold Hardiness in Laboratory Experiments
In order to understand how quickly the adelgid can respond to the
onset of cold temperatures, we preconditioned the adelgids by hold-
ing them in Percival growth chambers for 3 or 7 d at one of three
different temperatures (2C (control), 12C, and 10C) before we
measured their supercooling points. To do this, branches containing
adelgid sistentes were collected from eastern hemlock trees in
Amherst, MA, on 20 January 2016. Supercooling points of these
adelgids were obtained using the methods described above. Data
from this experiment were analyzed by ANOVA coupled with one-
sided T-tests to determine the statistical difference between the
supercooling points of the 12C and 10C preconditioning treat-
ments from the controls. We also regressed the supercooling points
versus exposure temperature for each of the two durations. The ana-
lyses were conducted in R (R Core 2012).
There was a seasonal trend evident in the supercooling points of
adelgids from northern locations (Fig. 2A), wherein they were much
lower in February 2015 than in March 2015 or December 2015
(Table 2). The coldest temperatures of the year typically occur in
January or February (Table 2). At northern sites, supercooling
points were much lower in February 2015, than they were in
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February 2016 (Fig. 2A). No such trends were evident in the south-
ern locations (Fig. 2B). There was a corresponding difference in
mean temperatures between the 2 yr, particularly in the 10 d preced-
ing the February samples (Table 2). At the three northern interior
sites (Fig. 1;Table 2), the difference was 9.8–10.5C warmer during
this period in 2016 compared with 2015. In contrast, the tempera-
tures at the southern sites were 2.9–0.2C colder in 2016 than in
2015 during this same period (Table 2). At the northern coastal site
in Wareham, MA, which is in the same hardiness zone (6B) as the
two Virginia sites, the early February temperature was 7.28C
warmer in 2016 than 2015 (Table 2), and the difference in super-
cooling points was correspondingly intermediate (Fig. 2A). The sites
presented in Fig. 2 and Table 2 were those for which we had ob-
tained samples from at least three, if not four, of the four different
sample months.
There was a significant positive correlation (Table 3) between
the supercooling points of adelgids and the average coldest yearly
temperature over the past 10 yr at the site of collection in February
2015 (Fig. 3A), March 2015 (Fig. 3B), December 2015 (Fig. 3C),
and February 2016 (Fig. 3D). The slope of the regression line for
February 2015 (Fig. 3A; Table 3) was significantly steeper than the
slope for February 2016 (Fig. 3D; Table 3), because of the much
lower supercooling points at the northern sites in February 2015. In
each of these samples, we tested 20–50 adelgids and there was al-
ways a large variation of supercooling points spanning at least 10C
at most locations, as is evident throughout (Fig. 3). This was true
even though all the adelgids in each sample typically came from the
same hemlock twig or twigs.
In the laboratory induction experiment using hemlock woolly
adelgids collected from around Amherst, MA, in January 2016, we
found that the supercooling point of adelgids increased with precon-
ditioning temperatures of 12C, 2C, and 10C(Fig. 4;df
¼2,331; F¼26.35; P<0.001; Table 3) after an exposure of only
3 d. A one-sided t-test showed that the mean supercooling points of
Fig. 1. Hemlock woolly adelgids collection locations plotted on a USDA plant cold-hardiness zone-maps based on average minimum winter temperatures
(1976–2006). Site numbers from Table 1 are given inside yellow circles.
Environmental Entomology, 2016, Vol. 0, No. 0 3
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adelgids in the 12C treatment were lower than adelgids in the
2C treatment (t¼4.561; df ¼203; P<0.0001), which were lower
than that for adelgids in the 10C treatment (t¼2.468; df ¼221;
P¼0.007). There was no change in the supercooling points among
adelgids held at these temperatures for 7 d instead of 3 d (Fig. 4;
df ¼1,331; F¼0.206; P¼0.65; Table 3).
Our laboratory demonstration of induction of cold hardiness among
adelgids exposed to 12C in as little as 3 d showed that adelgids
can acclimate to cold temperatures by lowering their supercooling
points over this time interval. It is important to note that this change
Table 1. Location, latitude, longitude, plant hardiness zone, average daily minimum winter (December–February) temperature over the past
30 yr, and average absolute minimum each year over the past 10 yr at different hemlock woolly adelgid collection sites
Site no. Site location State Latitude Longitude Hardiness zone Mean min. daily temp (C) Mean absolute winter min. (C)
1 Kentland Virginia 37.20747 80.5894 6B 1.2 15.7
2 Hiawasee Tennessee 35.16148 84.4817 6B 1.9 13.0
3 Helen Georgia 34.78576 83.75800 7B 2.1 12.5
4 Bent Creek, North Carolina 35.46545 82.65554 7A 3.8 13.8
5 Powhatan Virginia 37.60162 77.76826 7A 4.7 14.4
6 Blacksburg Virginia 37.39543 80.41462 6B 5.1 16.2
7 Wareham Massachusetts 41.76437 70.71539 6B 5.2 18.7
8 Hamden Connecticut 41.38869 72.90330 6B 5.4 19.0
9 Kingston Rhode Island 41.48076 71.52256 6B 5.6 21.9
10 Del. Water Gap Pennsylvania 40.92925 75.14279 6B 7.8 21.9
11 Taughannock Falls New York 42.53611 76.61154 5B 7.9 23.9
12 Quabbin Massachusetts 42.27940 72.34807 5B 8.3 21.8
13 Amherst Massachusetts 42.39208 72.53099 5B 8.7 22.7
14 Shelburne Falls Massachusetts 42.60424 72.73312 5B 9.5 22.3
15 Mine Kill New York 42.43328 74.46283 5B 9.7 25.5
Freezing temperature oC
A : North
B : South
c c
c b b
a ab b a a a
b b b
Fig. 2. Mean (þSE) supercooling points of hemlock woolly adelgids collected from selected northern and southern locations in December 2015, February 2015,
February 2016, and March 2015. Within each site, mean supercooling points that share the same lower case letter are not statistically different from other sample
dates (one-way ANOVA, Tukey’s HSD test, a¼0.05).
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in cold hardiness was not due to killing off the least cold hardy
amongst the test adelgids. The lowest preconditioning temperature
(12C) used in this experiment (Fig. 4) was above the highest
supercooling point of the adelgids from this region (Fig. 4 and site
13 in Fig. 3D). Despite these changes in supercooling points, there
appeared to be no reduction in the variance of supercooling points
either in the laboratory (Fig. 4) or in the field (compare February
2016 with February 2015 or December 2015; Fig. 3). If the cold
hardiness evident in February 2015 or at 12C in the laboratory
(Fig. 4) were due to prior death of the least cold-hardy individuals,
then we would expect to see a decline in the variance of supercooling
points of those samples compared to the earlier dates or higher tem-
perature samples. That did not happen, as is evident in Figs. 3 and 4.
Compared to the big differences in supercooling points between
northern and southern adelgids evident in February 2015, the north
to south differences in February 2016 were much smaller than those
in February 2015, after a much milder January and early February.
Indeed, there had been almost no change in supercooling between
December 2015 (Fig. 3A) and February 2016 (Fig. 3D), and these
were about the same magnitude shown in the common garden ex-
periment in December 2015 (Lombardo and Elkinton, unpublished
data). The implication is that the induction of supercooling evident
in our data accounted for much of the north to south differences evi-
dent in February 2015 compared with February 2016.
The mean values of the coldest day of the year over the past
10 yr at each site (Table 1) were comparable with the supercooling
points recorded in February 2015 (Fig. 3A). The large variation in
supercooling points evident at all sites suggests that some adelgids
would die everywhere nearly every winter due to cold temperatures.
That conclusion is consistent with previous reports of north–south
variation in overwintering mortality of the adelgid (Trotter and
Shields 2009).
The supercooling points of adelgids from different sites in
December 2015 were essentially indistinguishable from those we
measured at the same time in adelgids from these same sites and
reared for two generations in a common garden experiment in west-
ern Massachusetts (Lombardo and Elkinton, unpublished data).
Our results from the common garden experiment show that adelgids
have evolved cold tolerance, as they have moved north from the site
of introduction near Richmond, VA, in the 1950s (Havill et al.
2006) and invaded New England in the late 1970s (McClure 1989,
1991). These results confirm those from the common garden experi-
ment conducted by Butin et al. (2005), who showed that adelgids
collected from three sites in eastern Maryland (hardiness zone 7A)
had lower cold hardiness based on survival from laboratory cold
shock after they were reared for two generations on adjacent trees
near Amherst, MA, compared with those collected and reared from
sites in Massachusetts (hardiness zones 6A and 5B). The implication
is that cold hardiness of the adelgid has a genetic basis. Butin et al.
(2005) argued that evolution of cold hardiness in this insect was pos-
sible despite its parthenogenetic reproduction in North America, be-
cause of the vast numbers of adelgids present. These genetic
differences thus form the baseline of north–south differences in cold
hardiness evident in December 2015 (Fig. 3A).
Table 2. Mean winter temperatures by month and mean tempera-
tures during the first 10 d in February prior to February measure-
ments at select northern and southern sites in 2014–2015 and
Site Zone Month 2014–2015 2015–2016 Difference
Northern sites
Amherst, MA 5B Dec. 4.7 9.27 4.57
Jan. –1.09 2.38 3.48
Feb. –3.93 5.06 8.99
Feb. 1–10 –3.67 6.83 10.5
Mar. 4.05 11.08 7.03
Quabbin, MA 5B Dec. 4.71 8.49 3.78
Jan. –1.51 1.61 3.12
Feb. –4.48 4.23 8.72
Feb. 1–10 –4.56 6.28 10.84
Mar. 3.19 10.02 6.83
Tuag, NY 5B Dec. 2.58 8.76 6.18
Jan. –3.17 –0.22 2.95
Feb. –6.53 2.39 8.92
Feb. 1–10 –3.56 6.28 9.84
Mar. 1.4 9.75 8.35
Wareham, MA 6B Dec. 8.28 11.92 3.64
Jan. 2.4 4.26 1.86
Feb. –1.13 5.88 7.01
Feb. 1–10 –0.39 6.89 7.28
Mar. 4.34 9.82 5.48
Southern sites
Blacksburg, VA 6B Dec. 7.99 13.85 5.86
Jan. 4.78 3.59 –1.19
Feb. 2.9 5.75 2.85
Feb. 1–10 9.00 7.39 –1.61
Mar. 11.92 15.93 4.01
Kentland, VA 6B Dec. 7.53 13.64 6.11
Jan. 4.1 3.94 –0.16
Feb. 2.42 6.07 3.65
Feb. 1–10 7.37 7.17 –0.20
Mar. 11.83 15.63 3.8
Helen, GA 7B Dec. 10.38 13.69 3.32
Jan. 6.77 5.45 –1.33
Feb. 5.06 7.06 2.00
Feb. 1–10 9.22 6.28 –2.94
Mar. 14.41 15.57 1.16
Difference ¼(2015–2016 mea n) (2014–2015 mean).
Table 3. Regression coefficients of supercooling points estimated in different months plotted against average minimum winter temperature
(Fig. 3) or versus exposure temperatures in the laboratory (Fig. 4) and one-tailed T-tests for slopes <0
Date Figure Intercept (SE) Slope (SE)
T, slopes <0P-value
Feb. 2015 3A 9.02 (0.78) 0.675 (0.041)a 16.48 P<0.001
Mar. 2015 3B 12.82 (0.85) 0.415 (0.045)b 9.18 P<0.001
Dec. 2015 3C 16.25 (0.393) 0.103 (0.021)c 4.99 P<0.001
Feb. 2016 3D 13.78 (0.476) 0.272 (0.026)d 10.28 P<0.001
3-d exposure 4 19.591 (0.147) 0.080 (0.017) 4.823 P<0.001
7-d exposure 4 19.501 (0.135) 0.082 (0.015) 5.449 P<0.001
Different lower-case letters associated with slopes in Fig. 3 indicate they are significantly different from one another (Bonferroni-corrected Z-test, a¼0.05).
Environmental Entomology, 2016, Vol. 0, No. 0 5
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On 14 February 2016, a sudden cold event swept the northeast-
ern United States. As stated above, temperatures prior to that time
had been unusually mild and northern adelgids were much less cold
hardy (Figs. 2A and 3D; Table 2), than they had been the previous
winter. Temperatures at our research sites near Amherst, MA,
dropped to 24.4C. These temperatures were below the supercool-
ing points of nearly all adelgids from this region we had just tested
(Fig. 1C). We were thus not surprised to discover that nearly 100%
of these adelgids from our research sites in western Massachusetts
were dead. In contrast, overwintering mortality in these populations
was only 10–20%, when measured the previous week prior to the
cold event. We examined adelgids from other locations in New
England, including coastal sites in Massachusetts, Rhode Island, and
Connecticut, and also at our two sites in New York. Nearly 100%
Fig. 3. Supercooling points of hemlock woolly adelgids collected from 15 northern, coastal, and southern locations (Table 1)in(A) February 2015, (B) March 2015,
(C) December 2015, and (D) in February 2016 plotted versus mean minimum winter temperature (coldest temperature of the winter) over the past 10 yr (2006–
Fig. 4. Supercooling point of adelgids collected from Amherst, MA, on 20 January 2016 and held at 12C, 2 C, and 10 C for 3 and 7 d.
6Environmental Entomology, 2016, Vol. 0, No. 0
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of them were dead as well. The implications of this event are that
sudden declines in temperature following periods of warmer tem-
peratures can cause high adelgid mortality. These adelgids can adapt
to cold temperatures, if they are given sufficient time to do so. What
that timeframe is should be investigated in future experiments.
These observations are consistent with the findings of Paradis
et al. (2008), who reported that overwintering, adelgid mortality
was more highly correlated with variation in temperature than with
the absolute minimum temperature across a range of sites and years
(2004–2007) in Massachusetts. Before we conducted our study, we
knew from the work of Skinner et al. (2003) that adelgid cold hardi-
ness would vary from month to month over the winter. We assumed,
however, that these values would be the same from one winter to
the next in any population. Now we know that is not true. It de-
pends on prior exposure to cold temperatures, which varies from
winter to winter. The ability of this insect to survive winter tempera-
tures is a function of previous exposure to cold, which builds upon
the north–south genetic differences in cold hardiness.
We thank Mike Bohne, Juli Gould, Nathan Havill, Bryan Mudder, Andy
Tait, Joshua Pezet, Mark Mayer, Ryan Crandall, and Julia MacKay for col-
lecting and sending us hemlock woolly adelgid samples. We thank Sebastian
Harris, Jen Krassler, and Ryan Crandall for helping us with the supercooling
runs and Jeff Boettner and Katelyn Donahue for help with the figures. We
thank Matt Ayres for loaning us his supercooling machine. We thank Ryan
Crandall, Hannah Broadley, Jeff Boettner, and Aaron Weed for comments on
the manuscript. This project was supported by a cooperative agreement be-
tween the University of Massachusetts and the USDA Forest Service number
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... Cold temperatures in the northern introduced range can cause mortality of the overwintering A. tsugae sistens generation, leading to a temporary population reduction Skinner et al., 2003;Trotter III & Shields, 2009). Adaptation of increased cold tolerance and climate change leading to milder winters are expected to accelerate the northward spread of A. tsugae (Elkinton et al., 2017;Ellison et al., 2018;Paradis et al., 2008), increasing the need for early detection techniques. Reliable methods of rapid and scalable early detection of A. tsugae infestations are necessary for effective mobilization of resources to implement management strategies and increase their rate of success (Liebhold & Kean, 2019). ...
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Environmental DNA (eDNA) analysis can be a powerful tool for the early detection of invasive organisms. However, research on terrestrial eDNA detection from foliage surfaces has been limited. In this study, we developed methods to capture and detect eDNA using qPCR from an invasive forest pest, hemlock woolly adelgid (Adelges tsugae), and three of its biological control predators Leucotaraxis piniperda, Leucotaraxis argenticollis, and Laricobius nigrinus. We designed four highly efficient qPCR assays with a low limit of detection (1–10 copies/reaction). The assay targeting A. tsugae was species-specific. The assays targeting Le. piniperda, and Le. argenticollis were biotype-specific in addition to being species-specific demonstrating applications of eDNA analysis beyond species-level detection. The La. nigrinus assay also detected DNA from closely related and hybridizing Laricobius rubidus. The eDNA methods were evaluated against traditional detection methods. We collected foliage samples from three strata (bottom, middle, and top) of eastern hemlock trees to detect the presence of A. tsugae. The detection of the biological control predators was evaluated using western hemlock foliage samples collected from the predators' native range in western Washington. The eDNA methods had significantly higher positive detection rates (2.8–4.5 times) than conventional methods of all target species. The strata of sampling were not significant in determining the presence of A. tsugae infestation. The eDNA concentration positively correlated with the observed density for all species. This study demonstrates the efficacy of eDNA analysis as a more sensitive tool for early detection of A. tsugae and to track the establishment of its biological control predators. © 2022 The Authors. Environmental DNA published by John Wiley & Sons Ltd.
... However, there is no evidence of temperatures in the winter of 2018 or 2019 sufficiently cold or of long-enough duration to induce above-average HWA mortality. Laboratory studies have found that HWA in our study area can survive short-term exposure to temperatures as cold as −30°C (Parker et al. 1998, Elkinton et al. 2017. Complete (100%) HWA mortality is likely to result from a mean winter temperature of −5°C, 93 d with a minimum temperature below −10°C, or an absolute minimum winter temperature of −40°C (Paradis et al. 2008). ...
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Hemlock woolly adelgid (HWA; Adelges tsugae Annand (Hemiptera: Adelgidae)) is the cause of widespread mortality of Carolina and eastern hemlock (Tsuga caroliniana Engelmann and T. canadensis (L.) Carrière) throughout the eastern United States (U.S.). Since its arrival in the northeastern U.S., HWA has steadily invaded and established throughout eastern hemlock stands. However, in 2018, anecdotal evidence suggested a sharp, widespread HWA decline in the northeastern U.S. following above-average summer and autumn rainfall. To quantify this decline in HWA density and investigate its cause, we surveyed HWA density in hemlock stands from northern Massachusetts to southern Connecticut and analyzed HWA density and summer mortality in Pennsylvania. As native fungal entomopathogens are known to infect HWA in the northeastern U.S. and rainfall facilitates propagation and spread of fungi, we hypothesized high rainfall facilitates fungal infection of aestivating nymphs, leading to a decline in HWA density. We tested this hypothesis by applying a rain-simulation treatment to hemlock branches with existing HWA infestations in western MA. Our results indicate a regional-scale decline and subsequent rebound in HWA density that correlates with 2018 rainfall at each site. Experimental rain treatments resulted in higher proportions of aestivating nymphs with signs of mortality compared to controls. In conjunction with no evidence of increased mortality from extreme winter or summer temperatures, our results demonstrate an indirect relationship between high rainfall and regional HWA decline. This knowledge may lead to better prediction of HWA population dynamics.
... Cold-hardening in the MPB involves the production of antifreeze compounds, including glycerol, in response to thermoperiodic cues (Bentz and Mullins 1999, Fraser et al. 2017, Thompson et al. 2019, dynamic processes that occur with high energetic cost (Danks 1987, Lee 1989. Supercooling points in MPB, indicative of the extent of coldhardening, have been shown to differ geographically among populations in the field (Bentz and Mullins 1999), as has been observed in many other insect species with large geographic distributions (Kukal and Duman 1989, Shintani and Ishikawa 2002, Elkinton et al. 2017. However, studies on the degree of heritability and plasticity for this trait are limited, and absent for MPB. ...
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Predicting species response to climate change is a central challenge in ecology, particularly for species that inhabit large geographic areas. The mountain pine beetle (MPB) is a significant tree mortality agent in western North America with a distribution limited by climate. Recent warming has caused large‐scale MPB population outbreaks within its historical distribution, in addition to migration northward in western Canada. The relative roles of genetic and environmental sources of variation governing MPB capacity to persist‐in‐place in a changing climate, and the migratory potential at its southern range edge in the United States, have not been investigated. We reciprocally translocated MPB populations taken from the core and southern edge of their range, and simultaneously translocated both populations to a warmer, low‐elevation site near the southern range boundary where MPB activity has historically been absent despite suitable hosts. We found genetic variability and extensive plasticity in multiple fitness traits that would allow both populations to persist in a warming climate that resembles the thermal regime of our low‐elevation site. We demonstrate, for the first time, that supercooling points in MPBs are influenced both by genetic and environmental factors. Both populations reproduced with seasonally appropriate univoltine generation times at all translocated sites, and bivoltinism was not observed. The highest reproductive success occurred at the warmest, out‐of‐range low‐elevation site, suggesting that southward migration may not be temperature‐limited.
... An invasive insect, the hemlock woolly adelgid (HWA; Adelges tsugae), is currently bringing about distinct and lasting impacts on the forest structure of the eastern United States [2,3]. HWA is spreading northward as climate change warms New England winters and reduces the frequency of cold snaps, which are the major limiting factor to adelgid populations in the US [4][5][6][7][8][9][10][11]. As multiple time series of lidar data over HWA infested sites have become publicly available, new opportunities have emerged to track the spread of this insect infestation and to characterize its impacts on forest structure. ...
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The hemlock woolly adelgid (HWA; Adelges tsugae) is an invasive insect infestation that is spreading into the forests of the northeastern United States, driven by the warmer winter temperatures associated with climate change. The initial stages of this disturbance are difficult to detect with passive optical remote sensing, since the insect often causes its host species, eastern hemlock trees (Tsuga canadensis), to defoliate in the midstory and understory before showing impacts in the overstory. New active remote sensing technologies—such as the recently launched NASA Global Ecosystem Dynamics Investigation (GEDI) spaceborne lidar—can address this limitation by penetrating canopy gaps and recording lower canopy structural changes. This study explores new opportunities for monitoring the HWA infestation with airborne lidar scanning (ALS) and GEDI spaceborne lidar data. GEDI waveforms were simulated using airborne lidar datasets from an HWA-infested forest plot at the Harvard Forest ForestGEO site in central Massachusetts. Two airborne lidar instruments, the NASA G-LiHT and the NEON AOP, overflew the site in 2012 and 2016. GEDI waveforms were simulated from each airborne lidar dataset, and the change in waveform metrics from 2012 to 2016 was compared to field-derived hemlock mortality at the ForestGEO site. Hemlock plots were shown to be undergoing dynamic changes as a result of the HWA infestation, losing substantial plant area in the middle canopy, while still growing in the upper canopy. Changes in midstory plant area (PAI 11–12 m above ground) and overall canopy permeability (indicated by RH10) accounted for 60% of the variation in hemlock mortality in a logistic regression model. The robustness of these structure-condition relationships held even when simulated waveforms were treated as real GEDI data with added noise and sparse spatial coverage. These results show promise for future disturbance monitoring studies with ALS and GEDI lidar data.
... McClure (1991) showed that population fluctuations of HWA are characterized by a two-year boom and bust cycle governed by the interaction of HWA with its hemlock host. Other recent research has documented the impact of recent cold winter events that have decimated HWA populations over the entire eastern U.S. in certain years (Cheah, 2017;Elkinton et al., 2017;McAvoy et al., 2017;Tobin et al., 2017). These events may cause the boom and bust cycle to synchronize over the region, though it is not clear if this or other weather events are the cause for the observed low densities in 2018. ...
Hemlock woolly adelgid (HWA), Adelges tsugae Annand (Hemiptera: Adelgidae), has devastated eastern hemlock (Tsuga canadensis [L.] Carriere) in a major portion of its native range in eastern North America. Population dynamics of HWA in the absence of predators have been studied for decades. After many years and much effort directed towards rearing and releasing biological control agents to manage HWA, one of these agents, Laricobius nigrinus Fender (Coleoptera: Derodontidae), is now successfully established at significant densities at sites from the southern to the mid-Atlantic states of the eastern U.S. However, high densities of HWA still persist at many locations throughout the region and spread of HWA and associated damage to hemlock continues. Population models for HWA have suggested that even upwards of 90% predation on eggs laid by the overwintering sistens generation will have minimal effect in reducing the population densities of HWA, if HWA are at high density. In this study, we tested the ability of L. nigrinus to reduce HWA densities, and experimentally tested these model predictions to better understand what impact, if any, L. nigrinus has on HWA densities. By using predator exclusion cages at field sites with well-established populations of L. nigrinus, we were able to record HWA densities, fecundity, overwintering mortality, and predation by L. nigrinus, as well as the proportion of branch tips producing new growth on study trees. Using our field-collected data, we refitted the model in ways that allowed us to predict what population densities we could expect for the following summertime progrediens generation given previous HWA density and levels of L. nigrinus. In both years, we found that despite high rates (greater than 80% ovisac predation) of predation by L. nigrinus on uncaged branches compared to caged branches, there were no significant differences in subsequent densities of the HWA spring generation between caged and uncaged treatments, as predicted by our model. In 2018, our field-collected densities of the summer progrediens generation were lower than what was predicted by the model in both predator exclusion treatments, possibly due to the model not incorporating tree health and climatic factors. Simulation models of pest insect populations based on field-collected data such as fecundity, density, overwintering mortality, and predation, could prove to be important in informing researchers and managers about the role of the biological control agent in the population dynamics of the target host.
... Future work on cold hardiness should focus on the insect's ability to withstand sustained cold temperatures and the insect's lower lethal temperature to fully understand the cold hardiness of an insect. Elkinton et al. [38] found that in February 2015, December 2015, and February 2016, the average supercooling point of HWA acclimated at Kentland Farm in Blacksburg, VA ranged from approximately −16 to −18 • C. Despite the year-to-year variation of supercooling points, data suggest that HWA is more cold-tolerant than its predators. This implies that the lack of recoveries for Laricobius species after the polar vortex was not only due to the fact that there was a lack of prey to feed on, but also because some of the beetles themselves could not withstand the extreme cold weather. ...
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The hemlock woolly adelgid, Adelges tsugae Annand, is an invasive insect that threatens hemlock species in eastern North America. Several species from the genus Laricobius are predators of A. tsugae in its native areas of Asia and the western United States. Two Laricobius species have been released as biological control agents: Laricobius nigrinus Fender, and Laricobius osakensis Montgomery and Shiyake. Laricobius rubidus LeConte is an adelgid predator native to the Eastern United States, where it can feed and complete development on A. tsugae opportunistically. Laboratory assays were conducted to assess the cold hardiness of these three Laricobius species, including two distinct populations of L. osakensis, by measuring the supercooling points of each species from November 2016 through March 2017. This information may be useful for choosing the best-suited biological control agent for a particular region to control A. tsugae. There was a significant difference between the overall mean supercooling point of L. rubidus compared to the other Laricobius spp. There were also significant differences of supercooling points between L. rubidus and both strains of L. osakensis in January, and significant differences between L. rubidus and all other strains in February. L. rubidus appear better adapted to cold extremes in the eastern U.S. than imported Laricobius spp.
... Organisms in poleward environments must cope with both cooler average temperatures and greater thermal fluctuation across diurnal and seasonal timescales (Marshall and Sinclair 2012). In ectotherms, these patterns of temperature fluctuation are associated with distinct physiological response mechanisms (Terblanche 2006;Hadamová and Gvoždík 2011;Elkinton et al. 2017;Noh et al. 2017). Constitutive cold resistance provides increased protection from continuous or unpredictable cold stress (Teets et al. 2011) but is energetically expensive and can depress individual growth rates (Marshall and Sinclair 2012). ...
Geographic variation in low temperatures at poleward range margins of terrestrial species often mirrors population variation in cold resistance, suggesting that range boundaries may be set by evolutionary constraints on cold physiology. The northeastern woodland ant Aphaenogaster picea occurs up to approximately 45°N in central Maine. We combined presence/absence surveys with classification tree analysis to characterize its northern range limit and assayed two measures of cold resistance operating on different timescales to determine whether and how marginal populations adapt to environmental extremes. The range boundary of A. picea was predicted primarily by temperature, but low winter temperatures did not emerge as the primary correlate of species occurrence. Low summer temperatures and high seasonal variability predicted absence above the boundary, whereas high mean annual temperature (MAT) predicted presence in southern Maine. In contrast, assays of cold resistance across multiple sites were consistent with the hypothesis of local cold adaptation at the range edge: among populations, there was a 4-min reduction in chill coma recovery time across a 2° reduction in MAT. Baseline resistance and capacity for additional plastic cold hardening shifted in opposite directions, with hardening capacity approaching zero at the coldest sites. This trade-off between baseline resistance and cold-hardening capacity suggests that populations at range edges may adapt to colder temperatures through genetic assimilation of plastic responses, potentially constraining further adaptation and range expansion.
Winter‐season extreme minimum temperatures may play a major role in limiting population growth and spread of the hemlock woolly adelgid (HWA) (Adelges tsugae Annand) (Hemiptera: Adelgidae), an invasive sap‐feeding insect that has caused extensive mortality of hemlock trees (Tsuga spp.) in many eastern United States (US) forests. This atypical insect feeds throughout the winter but populations can sustain high mortality when winter‐season extreme minimum temperatures drop below ‐20 oC to ‐30 oC. Detection of HWA in Michigan during 2015 motivated interest in HWA winter survival in the US Great Lakes region. Here, we used the Parameter‐elevation Regressions on Independent Slopes Model (PRISM) gridded daily minimum temperature dataset to construct a 1981‐2018 climatology of extreme minimum temperatures in the Great Lakes region, the first such effort for this region. Metrics examined include absolute and mean annual extreme minimum temperatures (defined as the lowest daily minimum temperature during the study period and the study‐period mean lowest daily minimum temperature during each calendar year, respectively), and the frequency of daily minimum temperatures below ‐20 oC and ‐30 oC. Minimum temperature patterns we identified support the following two hypotheses: first, proximity to water, surface elevation, and latitude are the principal controls for extreme minimum temperatures in the Great Lakes region; second, the modifying influence of the relatively warm Lake Michigan serves to protect locations within about 10‐25 km of the lakeshore from severe and potentially lethal temperatures for HWA. Analysis of projected minimum temperatures at the end of the 21st century (2080‐2099) reveals a range of HWA distribution expansion scenarios. Although the original motivation for this study arose from interest in potential HWA mortality, a climatological study of extreme minimum temperatures has potentially broad relevance to, for example, human health and safety and forest ecology. This article is protected by copyright. All rights reserved.
The ability of a biocontrol agent to acclimate to and survive the climate of intended introduction locations is a critical attribute for successful biological control of an invasive pest. We evaluated the cold tolerance of Spathius galinae Belokobylskij & Strazanac, a braconid parasitoid native to the Russian Far East, introduced to the United States for biocontrol of the ash (Fraxinus spp.) pest, emerald ash borer (EAB), Agrilus planipennis Fairmaire, by measuring the supercooling point (SCP) of mature S. galinae larvae exposed to winter temperatures at four different field locations that span a gradient of plant hardiness zones. We observed a significant effect of overwintering location on SCPs of S. galinae larvae collected from field populations, with lower SCPs observed at locations with lower average minimum ambient temperatures. We also tested SCP of three stages (early-instar, late-instar, and mature cocooned larvae) of lab-reared parasitoids and found that SCP did not significantly differ between stages of lab-reared S. galinae. Our findings provide strong evidence that S. galinae can reduce SCP in response to below-freezing temperatures. The increase in cold hardiness of S. galinae in response to below-freezing temperatures should be considered in delineation of the optimal geographic range for biocontrol releases against EAB in North America.
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Climate change has been linked to shifts in the distribution and phenology of species although little is known about the potential effects that extreme low winter temperatures may have on insect host-parasitoid interactions. In late January 2019, northern regions of the United States experienced a severe cold wave caused by a weakened jet stream, destabilizing the Arctic polar vortex. Approximately 3 mo later at six study sites in southern Michigan and three in southern Connecticut, we sampled the overwintering larvae of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), and two larval parasitoids, Spathius galinae (Hymenoptera: Braconidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae), that are being introduced as emerald ash borer biocontrol agents in North America. At these nine study sites, emerald ash borer-infested ash trees and/or saplings were debarked and each overwintering emerald ash borer and parasitoid larva was then examined for cold-induced mortality, as indicated by a brown coloration, flaccid, and watery consistency. In early spring in Michigan, we found 4.5-26% of emerald ash borer larvae, 18-50% of S. galinae larvae, and 8-35% of T. planipennisi larvae were killed by cold. In Connecticut where temperatures were more moderate than in Michigan during the 2019 cold wave, <2% of the larval hosts and parasitoids died from cold injury. Our findings revealed that cold-induced mortality of overwintering larvae of emerald ash borer and its larval parasitoids varied by location and species, with higher mortality of parasitoid larvae in most Michigan sites compared to host larvae. The potential impacts of our findings on the management of emerald ash borer using biocontrol are discussed.
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Hemlock (Tsuga canadensis) plays a unique role in Eastern forests, producing distinctive biogeochemical, habitat, and microclimatic conditions and yet has begun a potentially irreversible decline due to the invasive hemlock woolly adelgid (Adelges tsugae; HWA) that causes foliar damage, crown loss, and mortality of host trees. Understanding the regional, landscape, site, and stand factors influencing HWA spread and impact is critical for predicting future landscape dynamics and directing effective management. Using aerial photographs, we documented hemlock distribution throughout central Massachusetts and subsampled 123 stands to examine the spatial pattern of HWA and its impact on tree vigor and mortality since its arrival in 1989. In the study region, over 86,000 ha of hemlock forest were mapped in 5,127 stands. White pine (Pinus strobus), red oak (Quercus rubra), red maple (Acer rubrum), and black birch (Betula lenta) were common overstory associates. Hemlock abundance increased from south to north, commonly on western and northwestern slopes. Average stand size was 55 ha, overstory basal area ranged from 23 to 55 m 2 ha À1 and overstory stem densities averaged 993 ha À1 . By 2004, 40% of sampled stands were infested, but most stands remained in good health overall; only 8 stands contained high HWA densities and only two had lost .50% overstory hemlock. Out of fifteen stand and landscape predictor variables examined, only latitude and winter climate variables were related to HWA density. Cold temperatures appear to be slowing the spread and impact of HWA at its northern extent as HWA infestation intensity and hemlock mortality and vigor were significantly correlated with average minimum winter temperature. Contrary to predictions, there was no regional increase in hemlock harvesting. The results suggest that regional HWA-hemlock dynamics are currently being shaped more by climate than by a combination of landscape and social factors. The persistence and migration of HWA continues to pose a significant threat regionally, especially in the northern portion of the study area, where hemlock dominates many forests.
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Hemlock woolly adelgid (HWA; Adelges tsugae Annand) infestations have resulted in the continuing decline of eastern hemlock (Tsuga canadensis (L.) Carriere) throughout much of the eastern United States. In 1994 and 2003, we quantified the vegetation composition and structure of two hemlock ravines in the Delaware Water Gap National Recreation Area. This is the first study to use pre-adelgid disturbance data, annual monitoring of infestation severity, and annual records of hemlock health to assess forest response to HWA infestation. In 2003, 25% of monitored hemlock trees were either dead or in severe decline. Measures of hemlock decline (crown vigor, transparency, density, and dieback) were correlated with HWA infestation severity and changes in light availability over the study period. Average percent total transmitted radiation more than doubled at these sites from 5.0% in 1994 to 11.7% in 2003. The total percent cover of vascular plants increased from 3.1% in 1994 to 11.3% in 2003. Species richness increased significantly, and more species were gained (53) than lost (19) from both ravine floras over the 9-year study period. Though exotic invasive plants were absent from these ravines in 1994, our 2003 resurvey found invasive plants in 35% of the permanent vegetation plots.
Understanding the seasonal phenology of an insect pest in a specific geographic region is essential for optimizing the timing of management actions or research activities. We examined the phenology of hemlock woolly adelgid, Adelges tsugae Annand, near the southern limit of the range of eastern hemlock, Tsuga canadensis (L) Carriere, in the Appalachians of northern Georgia, where adelgid phenology has not been previously reported. Adelges tsugaeinfested hemlock trees were visited at various sites from 2004 - 2007. Two hemlock twigs were collected from each of 3 hemlock trees per site, except during the final 3 months of sampling when 1 twig was collected from each of 3 trees per site. Progrediens adults initiated opposition by midMay, 2-4 weeks earlier than has been reported for more northern parts of the adelgid range. Sistens eggs were present until late-June (2006) or early-July (2004 - 2005). After aestivation, sistens nymphs resumed development by early October. Sistens adults were first found in early January and were present until midMay. Progrediens eggs were noted as early as February (2005 - 2007), were abundant in March and April, and persisted until midMay. Progrediens crawlers were present by early March and occurred throughout the next 2-3 months. Progrediens adults were found between midMay and late June. This information may be used to help optimize release of biological control agents to insure proper synchronization with adelgid life stages and to aid in collection of food for predator rearing facilities.
Question: Do invasive species adapt during range expansion? Data are few and many expect adaptation to be constrained by low genetic variation in invaders, which frequently experience population bottlenecks during colonization. Experimental results: We used a common-garden experiment to show that the invasive hemlock woolly adelgid (Insecta: Hemiptera: Adelgidae: Adelges tsugae) has evolved greater resistance to cold shock as it has expanded its range northward. This insect feeds on exposed twigs in winter and is vulnerable to extreme cold. Modelling results: Adelges tsugae has grown to a sufficiently large population size that its adaptive evolution appears unconstrained by the availability of new mutants, despite its parthenogenetic reproduction. Conservatively, its population size likely exceeds 1/(2u) within 40 ha of forest, where u is the haploid per-base mutation rate, so that on average a mutation arises each generation at every base pair in the entire genome within this area. Conclusion: This escape from genetic constraint is likely to be found in many species that have invaded successfully, facilitating their adaptation to novel conditions.
Hemlock woolly adelgid (HWA), Adelges tsugae, an introduced aphid-like insect from Asia, is expanding its range across the northeastern United States through the range of Tsuga canadensis (eastern hemlock) and can severely reduce or eliminate this important late-successional species. As part of a study investigating stand- and landscape-level forest dynamics resulting from HWA infestation, we examined initial community response of eight T. canadensis stands in south-central Connecticut. Our major objectives were to assess mortality patterns in T. canadensis, evaluate subsequent changes in stand microenvironment, and relate these and stand composition to initial patterns of regeneration, understory response, and community reorganization. Tsuga canadensis damage varied broadly across the study area ranging from near zero to greater than 95% mortality. All size and age classes sampled were attacked by HWA, although smaller trees exhibited higher mortality rates than larger trees. All remaining T. canadensis sampled in seven of the eight stands were infested with HWA and over 90% suffered at least 50% foliar loss. Substantial accumulations of downed woody debris have developed in stands with severe HWA damage. Canopy gaps created by HWA damage significantly increased the amount of light reaching the forest floor and resulted in rapid understory vegetation responses. Prolific Betula lenta (black birch) establishment occurred in stands with moderate to severe T. canadensis mortality. In addition, opportunistic herbaceous species (Erechtites hieracifolia, Phytolacca americana) and exotic species (Ailanthus altissima, Microstegium vimineum) have recently invaded these stands. Due to mortality from HWA, T. canadensis seedlings were scarce in sampled stands, suggesting that advance regeneration and seedbanks will not be important mechanisms for T. canadensis reestablishment. Tsuga canadensis cannot sprout following defoliation and has no apparent resistance to HWA. Therefore, dramatic reductions in T. canadensis across broad geographical areas appear imminent if HWA dispersal continues unimpeded and no effective natural enemies of HWA are found.
An earlier review in this journal (Baust and Rojas, 1985) encouraged investigators to “critically reassess” much of the “generally accepted dogma” which characterises research on insect cold hardiness and to undertake an assessment of the “founding hypotheses” of the subject. In their contribution Baust and Rojas considered the factors which may influence the classification of a species as freezing tolerant or intolerant (supercooling point, optimal cooling/ warming rates, state of adaptation and methods of determining survival) and summarized the observations which challenge the consensus view which identifies the gut as the probable prime site for -ice nucleation in freezing-intolerant species. The likelihood of death for an individual insect from the effects of cold depends on (i) the cold hardiness of the specimen and (ii) the temperatures and periods of exposure experienced in the overwintering site. The interaction between these two factors will determine the proportion of a population that lives or dies. it is important to recognise that the term cold hardiness refers to the combined attributes required by an insect to overcome the various deleterious effects of low temperature. Viewed from an ecological perspective insect cryobiology is therefore concerned with all the events and processes governed by low temperature which influence and ultimately determine survival or mortality in the natural environment. In practise, research over 50 years has concentrated on the physiological and biochemical mechanisms of surviving or avoiding freezing while largely disregarding the possibility that for some or many species (studied or unstudied) other injurious effects of cold may be a more important threat to life. Additionally much of this work on cold hardiness has been based on laboratory temperature regimes which take no account of ecological aspects such as behaviour, overwintering site microclimate and the inter