ArticlePDF Available

Gloomy Scale (Hemiptera: Diaspididae) Ecology and Management on Landscape Trees

Authors:

Abstract and Figures

Gloomy scale, Melanaspis tenebricosa (Comstock), is native to the eastern United States and feeds on deciduous trees. In natural areas, it is a background herbivore that typically remains at low densities. Gloomy scale generally responds positively to warming with greater egg production, size, survival, and abundance. In urban areas, which are warmer than surrounding natural areas, gloomy scale is pestiferous on planted trees, particularly red maple (Acer rubrum L.; Sapindales: Sapindaceae) but other native maples as well. They live on the bark and damage host trees by feeding from plant cells and tissues, which deprives the trees of energy and nutrients, reducing the trees’ growth and overall health. Gloomy scales are likely to expand their range beyond the Southeast and become pestilent in new areas with continued climatic warming and urbanization. Here we present a review of the biology, ecology, response to environmental conditions, host range and damage, and management of gloomy scale.
Content may be subject to copyright.
1
Journal of Integrated Pest Management, (2020) 11(1): 24; 1–9
doi: 10.1093/jipm/pmaa028
Profile
© The Author(s) 2020. Published by Oxford University Press on behalf of Entomological Society of America.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/
licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For
commercial re-use, please contact journals.permissions@oup.com
Gloomy Scale (Hemiptera: Diaspididae) Ecology and
Management on LandscapeTrees
MichaelG.Just,1,2,4, AdamG.Dale,3 and StevenD.Frank1,
1Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695, 2Current address: U.S. Army
ERDC CERL, Champaign, IL 61826, 3Entomology and Nematology Department, University of Florida, Gainesville, FL 32611, and 4Cor-
responding author, e-mail: michael.g.just@usace.army.mil
Subject Editor: DavidCoyle
Received 28 September 2020; Editorial decision 20 November 2020
Abstract
Gloomy scale, Melanaspis tenebricosa (Comstock), is native to the eastern United States and feeds on deciduous
trees. In natural areas, it is a background herbivore that typically remains at low densities. Gloomy scale generally
responds positively to warming with greater egg production, size, survival, and abundance. In urban areas, which
are warmer than surrounding natural areas, gloomy scale is pestiferous on planted trees, particularly red maple
(Acer rubrum L.; Sapindales: Sapindaceae) but other native maples as well. They live on the bark and damage
host trees by feeding from plant cells and tissues, which deprives the trees of energy and nutrients, reducing the
trees’ growth and overall health. Gloomy scales are likely to expand their range beyond the Southeast and become
pestilent in new areas with continued climatic warming and urbanization. Here we present a review of the biology,
ecology, response to environmental conditions, host range and damage, and management of gloomy scale.
Key words: impervious surface, red maple, sleeper species, street tree, urban ecology
Gloomy scale, Melanaspis tenebricosa (Comstock), is a native
herbivore of trees in the southeastern United States. In forests,
gloomy scale is generally an innocuous herbivore found at low
densities. However, gloomy scale has been recognized as a major
pest of red maples planted along streets and in landscapes for over
a century (Metcalf 1912). Metcalf (1922) remarked that gloomy
scale ‘without exception was the most important pest of shade
trees in North Carolina’. This remains the case (Frank 2019)
as recent work has documented populations of gloomy scale at
damaging adult female densities of up to 70/cm in urban areas
from Florida to Delaware (Just et al. 2018, Long et al. 2019,
Frank and Just 2020).
Yet, no peer-reviewed papers were published on gloomy scale be-
tween 1923 and 2013. Since 2013, renewed recognition of gloomy
scale as a critical pest has led to new research, peer-reviewed papers,
management tactics, and extension resources.
It can take 6–10 yr for gloomy scales to reach damaging densities
on a host (Backe and Frank 2019), and it often goes unnoticed until
very high densities or symptoms of declining tree condition are pre-
sent. Like other armored scale insects, gloomy scale is difcult to
manage with insecticides once infestations become severe. The time,
effort, and cost to rectify severe gloomy scale infestations may out-
weigh the value of the infested tree. However, cultural integrated
pest management (IPM) tactics have recently been developed to help
identify appropriate planting sites for susceptible trees and reduce
gloomy scale infestations and damage. These IPM tactics include
using impervious surface thresholds to identify suitable locations
(Dale etal. 2016, Just etal. 2018), providing supplemental water to
reduce tree stress and gloomy scale tness (Dale and Frank 2017),
and considering differences in cultivar susceptibility (Lahr et al.
2020). Like many other scale insects, gloomy scale density and fe-
cundity increase with ambient warming, both in cities (Dale and
Frank 2014a) and forests (Youngsteadt etal. 2015, Frank 2020).
Moreover, gloomy scale exhibit many qualities of sleeper species—
species that remain quiescent until environmental change leads to
population surges—signaling the potential for continued pestilence
within its current range. With continued warming and urbanization,
gloomy scale is likely to expand their range beyond the Southeast and
potentially invade forests (Frank and Just 2020). Our understanding
of gloomy scale biology, IPM, and response to global change has ad-
vanced signicantly in the past 8 yr. However, gloomy scale remains
the dominant pest of urban red maples in the Southeast and is likely
to become worse in new regions.
Life Stages
Gloomy scale, like many scale insects (Hemiptera: Coccoidea), is sexu-
ally dimorphic. These differences are noticeable in the second instar
and become more apparent as the insect matures (Metcalf 1922).
Female gloomy scales are neotenic and molt twice, whereas males molt
applyparastyle "g//caption/p[1]" parastyle "FigCapt"
applyparastyle "g" parastyle "Figure"
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
2 Journal of Integrated Pest Management, 2020, Vol. 11, No. 1
four times before developing into winged adults as is common among
armored scale species (Baranyovits 1953). The length of the gloomy
scale lifecycle is approximately 1 yr for females and 4 mo formales.
Adults
Gloomy scales are covered ventrally and dorsally by an armored
covering called a test (Fig.1). The ventral test is at, white in the center
and black around the edge, and attaches to the bark of the host tree
(Comstock 1881, Metcalf 1922). Gloomy scale, like other armored
scales, feed on uids from parenchyma cells with piercing-sucking
mouthparts (Beardsley and Gonzalez 1975). The dorsal test (hence-
forth referred to as test) is convex and typically gray with a black spot
surrounded by a white ring. This spot is off-center of the female test and
the near anterior edge of the male test. Coloration is variable and can
be inuenced by the bark color of the plant to which they are attached.
This contributes to the difculty in detecting gloomy scale infestations.
In many cases, individual gloomy scale will become embedded in the
epidermal bark layer, making detection even more difcult.
The soft body of adult female gloomy scales are nearly round
and measure 1–1.5mm long from their pygidium (fused abdominal
segments) to the anterior end of their body (Metcalf 1922, Deitz and
Davidson 1986, Dale and Frank 2014b). They are slightly convex
and are pale cream to dark pink (Fig. 1). Female gloomy scales
lack antennae, eyes, legs, and wings, and their body segmentation
is unpronounced. Adult females are morphologically juvenile save
mature sexual organs. Including their tests, they are up to 2mm in
diameter (Frank and Dale 2015).
Adult males, like many other armored scale species, are winged
and mobile equipping them to nd mates. Male bodies and tests are
oblong and are shorter than females with an average test length of
0.9 mm and a body length of 0.75 mm, including their aedeagus
(male reproductive organ). This accounts for up to 1/2 of the total
body length in males (Metcalf 1922, Kosztarab 1987, Gullan and
Kosztarab 1997). They have distinct body segmentation and ap-
pendages, though their mouthparts are nonfunctional. The male
wingspan is approximately twice their length (Metcalf 1922).
Eggs
Gloomy scale eggs are oval, translucent to pink, and, on average,
measure 0.25mm long and 0.15mm wide once fully developed
(Miller and Davidson 2006, Dale and Frank 2014c; Fig. 2).
Because scale insect bodies are translucent, a gravid adult female’s
eggs can be seen within her body through her exoskeleton (Fig.3).
Eggs are never seen outside of the body because gloomy scales
are ovoviviparous, meaning eggs are held within the female body
until eclosion, at which point rst-instar nymphs (called crawlers)
emerge from the female to feed. An adult female will produce
10–70 eggs, which eclose and disperse continuously over 6–8wk
(Dale and Frank 2014b).
Fig. 1. Gloomy scale adult female (pink) with dorsal test removed. The
white center and black outer ring of ventral test can be seen under the soft-
bodied female. Intact dorsal tests of gloomy scales of various life stages
are also shown. Gloomy scale (Diaspididae: Melanaspis tenebricosa) Matt
Bertone, https://www.flickr.com/photos/76790273@N07/8631555279, 2013, by
permission of Matt Bertone.
Fig. 2. Slide-mounted eggs extracted from a gloomy scale. Photograph by
Adam Dale.
Fig. 3. Eggs can be seen as darkened ovals through the exoskeleton of
an adult female gloomy scale immediately prior to crawler emergence.
Photograph by Adam Dale.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
Journal of Integrated Pest Management, 2020, Vol. 11, No. 1 3
Nymphs
Armored scale insect postembryonic development includes three in-
stars for females and ve for males (Beardsley and Gonzalez 1975,
Gullan and Kosztarab 1997). Female and male rst-instar gloomy
scales (Fig.4) are free moving with three pairs of legs, a pair of an-
tennae, and a pair of eyes (Metcalf 1922, Beardsley and Gonzalez
1975). Crawlers are oval, cream to pale orange, and have an average
length of 0.24mm and width of 0.17 (Metcalf 1922). Upon settling
on the host plant, gloomy scales tuck in their legs and antennae and
begin developing tests. The tests of armored scales are initially pro-
duced from wax secreted from wax secreting ducts and other mater-
ials, then later becoming composed of intermediate instar exuviae
and excrement (Takagi and Tippins 1972, Stoetzel 1975, Kosztarab
1987). The dark spot on gloomy scale tests is the former instar ex-
uviae (Frank etal. 2013).
Second-instar females are wingless and legless, remaining mor-
phologically juvenile for the duration of their life. The nal shape of
the female test after the second molt contains an opening referred to
as a crawler escape ap (sensu Kosztarab 1987) that provides access
for mating and for crawlers to exit. Toward the end of the second
instar, male armored scales begin to elongate and develop eye spots
and appendages. As with other armored scales, male gloomy scales
continue development with a third-instar pre-pupal and fourth-
instar pupal stage. Males do not develop functional mouthparts as
they do not feed after the second instar. Armored scales only develop
tests during feeding stages. Female tests contain rst- and second-
instar exuviae, whereas males only contain exuviae from the rst
instar (Beardsley and Gonzalez 1975).
Biology andEcology
Gloomy scales have one generation per year (Metcalf 1922, Stoetzel
1975) and overwinter as mated adult females (Deitz and Davidson
1986). Females begin oviposition in spring, around March in central
Florida, the southern end of their range, and May in central North
Carolina. Oviposition continues through early summer (June–July),
depending on the climatic conditions of the geographic location
(Stoetzel 1975, Dale and Frank 2014b). Female scales produce ve
to seven eggs per day over 6–8wk (10–70 total eggs) and crawlers
become active shortly after (Metcalf 1922, Stoetzel 1975, Dale and
Frank 2014b). Crawlers emerge from maternal tests and settle upon
the bark of the host tree’s stem or branches. Settling usually occurs
within a 30-cm distance (Metcalf 1922) and often within just a few
centimeters (Frank and Just 2020). Additionally, some crawlers will
settle beneath the maternal test (Stoetzel 1975). Coincident with set-
tling, crawlers insert their piercing-sucking mouthparts into the host
bark to begin feeding and secreting the wax and other materials that
becomes the test. The remaining immature stages are sessile, and fe-
males remain in this location for their lifetime. Males live several
hours to 2 d (Beardsley and Gonzalez 1975, Kosztarab 1987). Male
armored scales are generally thought to emerge around the same time
that females become sexually mature (Beardsley and Gonzalez 1975).
Gloomy scales reproduce sexually and through parthenogenesis.
Parthenogenesis may be more common in gloomy scales as early re-
searchers had difculties nding males (Comstock 1881, Metcalf
1912). Relative rates of sexual or parthenogenic reproduction are
unknown, though environmental conditions, such as temperature,
may affect sex ratio (Hughes-Schrader 1948, Alstad and Edmunds
1983). When mating, male gloomy scales insert their aedeagus
through the crawler ap in the female test. It is reported that female
armored scales only mate once, though males can mate with sev-
eral females during their adulthood (Beardsley and Gonzalez 1975,
Kosztarab 1987).
Active dispersal of gloomy scale crawlers is mostly contained to
the host tree where they are born. Some crawlers may migrate onto a
new host tree if twigs or branches are touching. Based on the infest-
ation of new isolated trees, gloomy scale crawlers are likelypassively
dispersed by wind, as has been documented for some other armored
scale species (Strickland 1950, Greathead 1972). Some armored
scales (Hemiptera: Diaspididae) disperse via phoresy (traveling on
another organism) on birds (Magsig-Castillo etal. 2010). The move-
ment of infested plant material by humans has also been linked to
the dispersal of scale insect species (Beardsley and Gonzalez 1975).
However, evidence suggests that this is not a primary mechanism for
gloomy scale introduction (Backe and Frank 2019).
Distribution
Gloomy scale has been recorded in at least 24 U.S.states, Tabasco,
Mexico, Panama, and the Galapagos Islands (Metcalf 1922, Deitz
and Davidson 1986, Lincango et al. 2010, García Morales et al.
2016). Their primary distribution is in the United States, and they
have been regularly recorded from Maryland to Florida and west to
Texas (Ferris 1941, Johnson and Lyon 1976, Waltman etal. 2016).
Gloomy scales are one of the most important ornamental tree pests
in the mid-Atlantic and southeast United States (Frank 2019), with
greatest densities in the midlatitudes of the eastern U.S.distribution
(Just etal. 2018, 2019). The geographic range of gloomy scale is not
likely limited by dispersal or host availability, since red maples (Acer
rubrum L.; Sapindales: Sapindaceae)and other hosts are nearly ubi-
quitous. For example, the natural distribution of red maple, their prin-
cipal host, has one of the longest distributions of any eastern North
American tree species, extending from Florida to Newfoundland and
Labrador (Burns and Honkala 1990). Like most arthropods and scale
insects, the range of gloomy scale is related to their physiological tol-
erance to the environment (Calosi etal. 2010, Just and Frank 2020).
Mean overwinter survival was greatest for gloomy scales originating
in Raleigh, NC (92%) when compared with Newark, DE (23%) or
Gainesville, FL (34%), near the edges of its range (Just and Frank
2020). In laboratory experiments, gloomy scales from Raleigh assayed
at −4.7°C, the mean minimum January temperature in Newark, lasted
15.4h before reaching a mortality threshold of 50% (Just and Frank
2020). Gloomy scales are most tolerant of the thermal conditions in
Fig. 4. Adult female gloomy scale with dorsal test removed and crawler
emerging(10 units equal 1 mm). Photograph by Adam Dale.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
4 Journal of Integrated Pest Management, 2020, Vol. 11, No. 1
the middle of their primary distribution, near Raleigh, NC. This area
is where densities are greatest and winter temperatures rarely descend
below −1.0°C (Just etal. 2019, Just and Frank 2020).
Warming and Urbanization Effects on Biology
andEcology
Impervious surfaces, such as sidewalks, parking lots, and streets, in-
crease surface and air temperatures and reduce water inltration,
both of which can directly and indirectly increase gloomy scale
density (Frank 2020). Within cities, gloomy scale body size, repro-
ductive output, and survival is positively correlated with warmer
temperatures and the amount of surrounding impervious surface
cover (Dale and Frank 2014a, Youngsteadt et al. 2015, Dale et al.
2016). Gloomy scale is most abundant on host trees in the warmest
parts of cities (Dale and Frank 2014a, 2017) and those hosts with
a high proportion of circumjacent impervious surface cover (Dale
et al. 2016, Just etal. 2019). For example, gloomy scale density
was 300 times greater on red maples with the warmest canopy
temperatures versus those just 2.5°C cooler in Raleigh, NC (Dale
and Frank 2014a). Impervious surface cover and warmer temper-
atures often coincide with drought stress in trees, which has been
linked to sap-feeding insect tness (White 1984, Hanks and Denno
1993a, Koricheva etal. 1998, Huberty and Denno 2004). Dale and
Frank (2017) investigated how heat and water stress affect gloomy
scale fecundity and size by monitoring pairs of trees throughout the
Raleigh, NC urban heat island. Since impervious surface increases
temperature and water stress, one tree in each pair received supple-
mental water to reduce water stress. This allowed the researchers to
decouple the coincident effects of heat and drought caused by cir-
cumjacent impervious surface cover on scale biology and abundance.
They found that gloomy scales produced over 17% more embryos
on the warmest unwatered trees than the warmest watered trees, and
over 65% more than the coolest watered trees which were 2.5°C
cooler. Asimilar pattern was detected in scale body size. Although
the mechanisms behind this remain unknown, other studies indicate
that it may be linked to changes in tree nutrient availability (White
1984) or defenses (Herms and Mattson 1992).
Many scale insect species reach high and damaging densities
on urban trees (Raupp etal. 2010, Dale and Frank 2018). This has
frequently been attributed to reduced natural enemy abundance,
and thus biological control, in urban locations (Hanks and Denno
1993b, Tooker and Hanks 2000). Dale and Frank (2014b) investi-
gated the relative contribution of urban warming and urban natural
enemies on gloomy scale abundance to address natural enemy con-
trol in urban areas. They found that parasitoid abundance increased
with gloomy scale density on urban trees, but parasitism rates did
not. Instead, temperature was positively associated with gloomy
scale fecundity and density. Similarly, Long etal. (2019) found that
temperature, rather than natural enemies or biological control, was
a signicant predictor of gloomy scale density on red maple street
trees. Gloomy scale density was ve times greater than on red maples
in urban forest fragments that were 1.2°C cooler. As is true for other
urban plant pests (e.g., Speight etal. 1998, Shrewsbury and Raupp
2000, Raupp etal. 2012, Parsons etal. 2020), warming and subse-
quent gloomy scale outbreaks were a result of reduced vegetation
structure and increased impervious surface cover (Dale and Frank
2014b). The strength of this response to warming varies with lati-
tude along the eastern coast of the United States, where the strongest
responses are found in the areas with the greatest gloomy scale
densities. But the effects of impervious surface—a proxy for heat,
drought, reduced vegetation, and gloomy scale density—generally
hold true across the gloomy scale distribution (Just et al. 2018,
2019). Ambient temperature has been experimentally found to be
the primary driver of gloomy scale abundances (Dale and Frank
2014b, a).
Gloomy scales exhibit characteristics of a sleeper species. For ex-
ample, Youngsteadt etal. (2015) found that gloomy scale abundance
increased on rural forest trees and urban street trees with overall
climate warming and urban warming, respectively. This suggests
gloomy scale could become a more important forest pest in some
areas under climate change. However, red maple trees in cities hosted
nearly 200 times as many individuals per twig than those in rural
areas (Youngsteadt etal. 2015). This indicates other factors, such
as drought, might also be a contributing factor in increased gloomy
scale densities. Gloomy scales exhibit other invasive characteristics
with warming, including range expansion and asynchrony with nat-
ural enemies (Frank and Just 2020). Gloomy scale has been recorded
in cities at latitudes or altitudes that are higher than where they were
observed just a century ago (Metcalf 1922, Frank and Just 2020).
These areas now have warmer winters on average due to climate
change or urbanization. When assayed against several temperat-
ures, gloomy scales survived best at temperatures representative of
the middle locations of its range as compared to temperatures from
northern and southern range boundaries (Just and Frank 2020).
Thus, gloomy scale thermal tolerance suggests that recent northward
and upward expansion may be concurrent with range retraction in
the South, where densities are already low, if temperatures increase
beyond thermal tolerances (Just etal. 2019, Just and Frank 2020).
Host Range andDamage
Gloomy scale is a major pest of red maple, silver maple (Acer
saccharinum L.), and hybrids of the two called Freeman maples
(Acer × freemanii A.E. Murray) (Metcalf 1912, Johnson and Lyon
1976). Maples are among the most commonly planted trees in
North America (Raupp etal. 2006) especially in southeastern cities
(Frank 2019). Gloomy scale is also documented on hosts from at
least 28 woody plant genera (García Morales et al. 2016), which
include species such as sugarberry (Celtis laevigata Willd.), Osage
orange [Maclura pomifera (Raf.) C.K. Schneid.], white ash (Fraxinus
americana L.), tulip poplar (Liriodendron tulipifera L.), and lime
pricklyash [Zanthoxylum fagara (L.)Sarg.].
High-density infestations can encase twigs, branches, and trunks
darkening the color and creating a bumpy texture on the host. This
results in a ‘gloomy’ appearance (Figs.5 and 6; FrankandJust2020),
Fig. 5. Red maple twig heavily infested with gloomy scale. Photograph by
Adam Dale.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
Journal of Integrated Pest Management, 2020, Vol. 11, No. 1 5
which is not salubrious for the plant host or aesthetically appealing.
Damage usually manifests rst as twig and small branch dieback
and then as canopy thinning (Metcalf 1922, Dale and Frank 2014a).
With time, larger branches deteriorate which can expedite death
of the host. Although undocumented in gloomy scale, additional
damage may result from toxins in saliva that are transferred to the
host as is the case with California red scale (Aonidiella aurantii
Maskell) (Baranyovits 1953).
Red maples can have severe gloomy scale infestations and begin
to exhibit decline less than a decade after planting (Backe and Frank
2019). By then, gloomy scale densities are high, and intervention is
long, expensive, and does not guarantee that tree health, appear-
ance, or condition will improve. Even after reducing gloomy scale
infestations, dead scale insect tests remain on the trunk and stem,
prolonging the tree’s gloomy appearance. Young red maples do not
generally host high densities of gloomy scale, so management efforts
may be better spent on promoting tree establishment or attending to
more serious pests (Seagraves etal. 2013, Backe and Frank 2019).
Arborists and tree care professionals capture the combined
health and aesthetics of a tree using a metric called tree condition
ratings (Berrang etal. 1985, Dale and Frank 2014a). Trees are rated
on an ordinal scale of condition (e.g., excellent, good, fair, or poor
condition) which is based on factors such as canopy fullness, branch
dieback, leaf coloration, and damage. A tree in good condition
would typically have a full canopy, green leaves, and no damage.
Contrastingly, trees in poor condition may exhibit sections of the
canopy without leaves, chlorotic leaves, dead branches, and notice-
able damage to the trunk. Red maple condition rating is correlated
with gloomy scale density on branches and with circumjacent imper-
vious surface cover (Dale and Frank 2014a). Scale density on trunks
is less correlated with these factors. This may be due to thicker bark
of older trees, which may reduce ability of gloomy scales to feed.
Thus, trunk scale density could decline even as branch density in-
creases (Backe and Frank 2019).
Management of GloomyScale
Due to their small size and obscure coloration, gloomy scales are
often not detected until they reach damaging levels. In general, ar-
mored scale insects are notoriously difcult and expensive to manage
due to morphology that makes them difcult to detect and protects
them from contact insecticides (McClure 1977, Raupp et al. 2001,
Chong etal. 2009, Frank 2012). Gloomy scale is no exception and
may be more difcult to control than other armored scales. This is
because gloomy scale crawlers, the vulnerable stage targeted with in-
secticides, emerge gradually over several weeks instead of all at once.
Nurseries do not appear to be a signicant source of gloomy scale in
the landscape (Backe and Frank 2019). Thus, preventive tactics like
proper site selection, genotype selection, and tree maintenance are
the best management approach to reduce infestation of trees once
planted.
Scouting and Monitoring
Active scouting is necessary to nd gloomy scale infestations early.
This can be conducted throughout the year because the scales have
a 1-yr life cycle and are sedentary for most of it. Heavily infested
trees can be recognized from afar due to darkened bark and ‘gloomy’
appearance. To scout for gloomy scales, inspect the bark of twigs,
branches, and the trunk of trees for tests using a hand lens or other
magnication. Since tests of live and dead scales accumulate over
time, old growth may look heavily infested even if few tests belong
to live individuals. Tests remain on trees after scales die so it is ne-
cessary to ensure scales are alive before proceeding with interven-
tion measures. To estimate how rapidly the population is expanding,
inspect the previous year’s growth by locating the terminal bud
scars. The scales on this growth will only be from one generation
(Backe and Frank 2019). Monitor infested trees for crawler activity
from spring into early summer. Inspect branches visually or wrap
double-sided tape around an infested branch to ensnare crawlers.
Ayellow sticky card can also be placed within 15cm of an infested
twig and monitored regularly to see if crawlers have been captured
(Dale etal. 2020). Another option is to look for crawlers under the
test, which is useful on infested trees with test-encrusted branches
and trunks. Degree-day models are not currently available, but could
be developed to help estimate crawler activity dates with more preci-
sion. To determine whether scales are alive, turn over or remove the
test. The scale is alive if plump and pale yellow to pink or if liquid
leaks from the insect when crushed. Dead scale bodies are brown to
dark red and deated, and tests are dry and brittle.
Intervention Thresholds
Currently, intervention thresholds to trigger gloomy scale interven-
tion do not exist, but tree condition declines as scale density in-
creases (Dale and Frank 2014a, Just etal. 2018, Backe and Frank
2019). The odds of a tree transitioning from good to poor condition,
when rated with a binary arboricultural condition rating, increases
by 2.25 times for each additional scale per centimeter of twig (M.
G.Just and S.D. Frank, unpublished data). Therefore, it is important
to intervene as soon as gloomy scale infestations are detected, par-
ticularly if the host tree is or will be planted in a site that is likely to
exacerbate the infestation.
Cultural Management
Impervious surfaces increase canopy temperature, tree water stress,
and gloomy scale density. Planting sites that have greater amounts
of impervious surface have red maples in poorer health due to scale
infestation and physiological stressors (Just etal. 2018, Lahr etal.
2018). Thus, even though intervention thresholds do not exist,
impervious surface thresholds have been developed, as a cultural
management tactic, to identify optimal planting sites and guide man-
agement efforts. The most promising cultural management tactic is
to select a planting site that will not impose warmer temperatures
Fig. 6. Red maple street tree without a gloomy scale infestation (left). Red
maple street tree of similar size with a severe gloomy scale infestation (right).
Photographs by Adam Dale.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
6 Journal of Integrated Pest Management, 2020, Vol. 11, No. 1
or water stress on the tree. Red maples planted in sites with less
than 36% circumjacent impervious surface (at a 20–25 m radius)
are those most likely to remain in good condition with low gloomy
scale infestations (Just etal. 2018). Trees in sites with 36–60% im-
pervious cover are likely to be in fair condition with moderate scale
infestations. It is not advisable to plant red maples at sites with
greater than 60% impervious surface due to the high likelihood of
severe gloomy scale infestation and resultant poor tree condition.
Trees in these sites would probably need regular intervention, such
as supplemental watering and insecticide applications, to prevent
their condition from deteriorating. Research is ongoing to establish
whether a tree can be rescued from heavy gloomy scale infestations
with intervention.
Impervious surface cover can be measured with digital tools such
as GIS or drafting software. For landscape professionals and other
practitioners without access to these tools, Dale etal. (2016) devel-
oped an on-site, pace-counting technique called Pace-to-Plant that
is used to estimate the amount of impervious surface at a planting
site (Fig.7). Briey, this technique requires that that an individual
walk four transects that originate at the planting site and are 90˚
apart from each other. The rst transect is selected as the one with
nearest impervious surface edge to the planting site, this transect is
oriented to cross the edge at a 45°. The individual takes 25 paces
(20–25 m) along each transect and sums the number of steps that
land on impervious surface. This total estimates the proportion (i.e.,
n steps out of 100)of impervious surface that is circumjacent to the
planting site. It is best to quantify the proportion of impervious sur-
face around a planting site during planning and design to determine
whether red maples are suitable and likely to thrive. Quantifying
impervious surface cover around trees already present in a landscape
is also useful to predict their potential for stress and gloomy scale
infestations. Tree planters and managers can use Pace-to-Plant along
with impervious surface thresholds to select red maple planting sites
throughout the southeastern United States (Dale et al. 2016, Just
etal. 2018).
High temperatures and water stress caused by impervious surface
cover combine to increase gloomy scale reproduction and density
on trees (Dale and Frank 2014b, 2017). Providing supplemental
water to red maples reduces water stress (measured as xylem water
potential) that results from high temperatures and drought condi-
tions caused by impervious surfaces (Dale and Frank 2017). Gloomy
scales on red maples in Raleigh, NC, that received 75 or 150 liters
of supplemental water each week during summer months produced
fewer embryos than scales on trees that did not receive supplemental
water. After 3 yr, red maples that received supplemental water had
70% fewer scales than trees that were not watered (S. D.Frank and
A.Dale, unpublished data). Thus, red maples growing in sites with
high impervious surface cover can be watered to slow gloomy scale
population growth to avoid severe infestations. By reducing water
stress and scale density, supplemental water could increase tree
growth and condition particularly in sites over the 36% impervious
surface threshold.
Tree selection, even among red maples, could be as important
as site selection in minimizing gloomy scale density and damage.
Dozens of red maple genotypes are available, including naturally
occurring wild types, at least 40 cultivated varieties, and several cul-
tivars of Freeman maples (Santamour and Mcardle 1980, Townsend
and Douglass 1998, Adkins etal. 2012). Red maple genotypes differ
in their susceptibility to gloomy scale infestation and in their resist-
ance and tolerance to other arthropod pests (Bentz and Townsend
2005; Seagraves etal. 2013; Prado etal. 2014; Prado etal. 2015a, b).
In both a common garden (Lahr etal. 2020) and observational study
(M. G.Just and S.D. Frank, unpublished data) of planted landscape
red maples, wild-type trees had lower gloomy scale densities than
cultivars or hybrids. For example, gloomy scale density on mature
landscape trees was 88% greater on hybrids than nonhybrid cul-
tivars and was 36.9-fold greater on hybrids than wild types. One
mechanism for these differences could be greater feeding site estab-
lishment or preadult survival on cultivar than wild-type red maples.
A climate chamber experiment revealed that establishment of
gloomy scale crawlers and the number of surviving adults was 15.2-
and 11.7-fold greater on cultivars than on wild-type red maples, re-
spectively (M. G.Just and S.D. Frank, unpublished data). However,
red maples exhibit high intraspecic variation and environmental
conditions can affect this variance. Agiven red maple type may per-
form better or worse depending on the local environment (Lahr etal.
2020). Most red maple cultivars and hybrids have not been evalu-
ated for susceptibility to gloomy scale, but wild types consistently
have lower gloomy scale densities and could be good alternatives
to cultivars in sites where strict uniformity is not required. As more
information becomes available, the most gloomy-scale-resistant red
maple that aligns with the desired tree characteristics for a planting
site should be used.
Biological Control and NaturalEnemies
There are at least ve species of parasitoid wasps of gloomy scale,
including wasps from the families Aphelinidae, Encyrtidae, and
Signiphoridae (Miller and Davidson 2006, Dale and Frank 2014b).
Several predators attack early-instar armored scale insects (Drea
and Gordon 1990). Natural enemies such as lacewings (Neuroptera:
Chrysopidae), ladybeetles (Coleoptera: Coccinellidae), and pre-
daceous midges (Diptera: Ceratopogonidae) may provide some
control of immature gloomy scales (Hanks and Denno 1993b,
Fig. 7. Illustration of the Pace-to-Plant technique as described in Dale etal.
(2016). Four transects, each 90° apart, originate at the tree planting site (white
filled circle) with the first transect at a 45° angle to the closest impervious
edge (i.e., curb). Each transect consists of 25 paces for a total of 100 paces.
The number of paces that land on impervious surface (white shoeprints) are
tallied to provide an estimate of the proportion of impervious surface cover
for that location. In this example, 67 paces land on impervious surface. At
67% impervious surface cover, a red maple planted at the location would
be expected to be in poor condition. Aerial image© 2020 Google adapted
by Adam Dale.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
Journal of Integrated Pest Management, 2020, Vol. 11, No. 1 7
Frank and Dale 2015). However, natural enemies may be unable
to control severe gloomy scale infestations in urban areas, where
warmer temperatures lead to high gloomy scale densities and low
vegetation complexity reduces natural enemy habitat availability
(Frank 2020). Long etal. (2019) found that natural enemy abun-
dances associated with landscape red maples were fourfold greater
than forest trees. They also found that gloomy scale densities were
ve times greater between landscape and forest trees, suggesting
that natural enemies do not suppress gloomy scale in urban loca-
tions where abiotic factors like heat and water stress drive scale
population growth (Long etal. 2019). In another study, Dale and
Frank (2014a) found that although parasitoid abundance increased
with gloomy scale abundance, parasitism rates remained constant
and the effects of warming on gloomy scale density and tness
eclipsed natural enemy control. Thus, biological control can only
serve as a part of the larger gloomy scale IPM program that starts
with planting location, genotype selection, and stress minimization.
Gloomy scale has also been observed to be colonized and killed
by redheaded fungus, Sphaerostilbe coccophila Tul. on urban trees
(Metcalf 1922). However, the frequency of scales killed by redheaded
fungus does not appear to provide appreciable control in the land-
scape (M. G.Just, personal observation; Metcalf 1922). Others have
attempted to use redheaded fungus as a biological control tool against
armored scale insect pests like San Jose scale (Quadraspidiotus
perniciosus Comstock) in orchards, but only found moderate con-
trol (Rolfs 1897). Moreover, the previous methods used to implement
redheaded fungus based biological control are not practical for use
on urban trees. Future work could explore strategies for manipulating
this fungus to provide gloomy scale suppression on urban trees.
MechanicalControl
There are no reported mechanical control trials with gloomy scale.
Though, it has been suggested that power washing or manually
scrubbing trees that have mild gloomy scale infestations could
help reduce scale density and remove unsightly tests from trees
(Frank and Dale 2015). These techniques have been used to remove
other tenacious scale species, including beech scale (Cryptococcus
fagisuga Lindinger) (Hempitera: Eriococcidae) (McCullough et al.
2005), calico scale (Eulecanium cerasorum Cockerell)(Hemiptera:
Coccidae) (Rieske et al. 2019), and crapemyrtle bark scale
(Eriococcus lagerstroemia Kuwana) (Borden et al. 2018), from
urban trees where insecticides were ineffective or impractical. The
power washing or scrubbing should be done when the tree is dor-
mant so that leaves are not damaged or in the way and at a pressure
that will not damage the bark or woody tissue of the tree.
Chemical Management
Published research on the chemical control of gloomy scale in the
landscape is minimal (Frank etal. 2013). Insecticides, like pyreth-
roids, that require direct or indirect contact with the target insect
for efcacy are generally not appropriate for armored scale man-
agement since they are immobile and protected by their tests. An
exception to this is when applications target crawlers which are not
protected by a test. However, this requires active monitoring to syn-
chronize applications with this life stage (Quesada etal. 2018). In
most cases, broad-spectrum insecticides like pyrethroids are a poor
choice for scale insect management. In fact, frequent applications of
broad-spectrum insecticides that leave toxic residues can increase ar-
mored scale density by killing natural enemies and preventing them
from recolonizing (Luck and Dahlstein 1975, McClure 1977, Raupp
etal. 2001, Frank etal. 2013).
Contact insecticides that do not leave a toxic residue, pri-
marily horticultural oils and insecticidal soaps, are also most ef-
fective against crawlers but can be effective against more mature
life stages (Quesada and Sadof 2017). Horticultural oil is more
effective than insecticidal soap since its chemical properties allow
it to more easily penetrate the waxy test (Quesada and Sadof
2017). Contact insecticides are most effective for armored scale
management when the duration of crawler emergence is short
and applications are made at peak crawler emergence (Quesada
etal. 2018). Gloomy scale is difcult to manage because crawlers
emerge a few at a time over a period of 6–8wk and may require
multiple insecticide applications, especially of products that re-
quire contact with the pest. Thus, systemic or translaminar in-
secticides may be more effective if the toxins are transported to
tissues on which gloomy scale is feeding. Research on other ar-
mored scaled insects has demonstrated the efcacy of horticul-
tural oils, systemic neonicotinoid insecticides, and insect growth
regulators against other armored scales but no research is avail-
able on gloomy scale (Sadof and Sclar 2000, Frank 2012, Xiao
etal. 2016, Quesada and Sadof 2017). However, some of the most
commonly used insecticides, belonging to the neonicotinoid class,
such as imidacloprid, clothianidin, and thiamethoxam, can also
have lethal and sublethal effects on natural enemies (Szczepaniec
etal. 2011, Calvo-Agudo etal. 2019), insect pollinators (Larson
etal. 2013), other benecial insects (Larson etal. 2012, Gan and
Wickings 2017), and be transmitted through food webs (Calvo-
Agudo etal. 2019, Frank and Tooker 2020, Quesada etal. 2020).
For this reason, it is important to consider the use of EPA-classied
reduced-risk translaminar or systemic products that are less
harmful to nontarget organisms. Moreover, since gloomy scales
and other armored scales feed intracellularly, systemic insecticides
may prove to be less lethal than they would be on phloem-feeding
pests like soft scales (Xiao et al. 2016). In result, management
can take longer to achieve and may require higher application
rates or more frequent applications when compared to soft scales
and other scale insect groups. Insecticide management is an area
where more long-term research is required.
Conclusion
Gloomy scale is a native insect that is an important pest of planted
red maples, among the most abundant ornamental and forest trees in
the eastern United States. It is likely to continue to be a pest in cities
and has the possibility to become a pest of natural areas with future
climatic warming since gloomy scale density tracks natural climate
patterns in forests and ts the criteria for a sleeper species (Frank
and Just 2020). Gloomy scale often goes unnoticed until infestations
are severe, at which point the time and expense to control the in-
festation may exceed the value of the tree. In landscapes, cultural
practices are the best approach to minimize gloomy scale damage
on newly planted red maples, including selecting wild-type trees or
less susceptible cultivars, installing in sites with limited amounts of
surrounding impervious surface cover, and providing maintenance,
particularly watering, that promotes red maple establishment and
minimizes stress. Employing these tactics will reduce the risk of
gloomy scale infestation and damage. As part of a gloomy scale IPM
program, assessing abiotic stress using the Pace-to-Plant method will
help identify trees prone to infestation and target management ef-
forts. Application of reduced-risk insecticides or horticultural oils
during periods of crawler activity is likely the best strategy to reduce
scale numbers and minimize risk to natural enemies on already in-
fested hosts. More work is needed to determine which red maple
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
8 Journal of Integrated Pest Management, 2020, Vol. 11, No. 1
cultivars are less prone to gloomy scale damage and how this might
vary with the local environment.
Acknowledgments
This work is supported by a Postdoctoral Fellowship (grant no. 2019-67012-
29633) from the U.S. Department of Agriculture, National Institute of Food
and Agriculture to M.G.J. Components of referenced and ongoing work by
S.D.F. have been supported by the U.S. Department of Agriculture, National
Institute of Food and Agriculture award numbers 2013–02476, 2016-70006-
25827, and 2018-70006-28914. We thank two anonymous reviewers who
provided critical feedback on this manuscript.
ReferencesCited
Adkins, C., S. Braman, M. Chappell, J.-H. Chong, J. Derr, W. Dunwell,
S. Frank, A.Fulcher, F.Hale, and W.Klingeman. 2012. IPM for select
deciduous trees in southeastern US nursery production. Southern Nursery
IPM Working Group, Knoxville, TN.
Alstad,D.N., and G.F.Edmunds, Jr. 1983. Selection, outbreeding depression,
and the sex ratio of scale insects. Science 220: 93–95.
Backe,K.M., and S.D.Frank. 2019. Chronology of gloomy scale (Hemiptera:
Diaspididae) infestations on urban trees. Environ. Entomol. 48:
1113–1120.
Baranyovits, F. 1953. Some aspects of the biology armoured scale insects.
Endeavour 12: 202–209.
Beardsley, J.W. Jr., and R.H. Gonzalez. 1975. The biology and ecology of
armored scales. Annu. Rev. Entomol. 20: 47–73.
Bentz, J.A., and A. M. Townsend. 2005. Diversity and abundance of leaf-
hopper species (Homoptera: Cicadellidae) among red maple clones. J.
Insect Conserv. 9: 29–39.
Berrang, P., D.Karnosky, and B.Stanton. 1985. Environmental factors af-
fecting tree health in New York City. J. Aboricult. 11: 185–189.
Borden, M., X. Martini, and A. Dale. 2018. Crapemyrtle bark scale,
Acanthococcus (= Eriococcus) lagerstroemiae (Kuwana) (Insecta:
Hemiptera: Eriococcidae). EENY-711. UF/IFAS Extension Publication,
Gainesville, FL.
Burns,R., and B. Honkala. 1990. Silvics of North America: 2.Hardwoods.
Agriculture Handbook 654. United States Department of Agriculture,
Forest Service, Washington, DC.
Calosi,P., D.T.Bilton, J. I.Spicer, S.C. Votier, and A.Ateld. 2010. What
determines a species’ geographical range? Thermal biology and latitu-
dinal range size relationships in European diving beetles (Coleoptera:
Dytiscidae). J. Anim. Ecol. 79: 194–204.
Calvo-Agudo, M., J. González-Cabrera, Y. Picó, P. Calatayud-Vernich,
A.Urbaneja, M. Dicke, and A.Tena. 2019. Neonicotinoids in excretion
product of phloem-feeding insects kill benecial insects. Proc. Natl. Acad.
Sci. USA 116: 16817–16822.
Chong, J. H., G. S. Hodges, and M. Samuel-Foo. 2009. First record and
management of the armored scale, Melanaspis deklei Dietz & Davidson
(Hemiptera: Diaspididae), in South Carolina. J. Agric. Urban Entomol. 26:
63–75.
Comstock, J. 1881. Report of the entomologist of the United States
Department of Agriculture for the year 1880. Government Printing Ofce,
Washington, DC.
Dale,A.G., and S.D.Frank. 2014a. The effects of urban warming on herbi-
vore abundance and street tree condition. PLoS One 9: e102996.
Dale,A. G., and S.D.Frank. 2014b. Urban warming trumps natural enemy
regulation of herbivorous pests. Ecol. Appl. 24: 1596–1607.
Dale,A.G., and S. D. Frank. 2014c. Urban warming trumps herbivore en-
emies. Bull. Ecol. Soc. Am. 95: 252–256.
Dale,A.G., and S.D.Frank. 2017. Warming and drought combine to increase
pest insect tness on urban trees. PLoS One 12: e0173844.
Dale,A.G., and S. D.Frank. 2018. Urban plants and climate drive unique
arthropod interactions with unpredictable consequences. Curr. Opin.
Insect Sci. 29: 1–7.
Dale,A.G., E.Youngsteadt, and S.Frank. 2016. Forecasting the effects of heat
and pests on urban trees: impervious surface thresholds and the ‘pace-to-
plant’ technique. Arboric. Urban For. 42: 181–191.
Dale,A.G., T.Birdsell, and J.Sidebottom. 2020. Evaluating the invasive po-
tential of an exotic scale insect associated with annual Christmas tree har-
vest and distribution in the southeastern U.S. Trees For. People 2: 100013.
Deitz, L., and J. Davidson. 1986. Synopsis of the armored scale genus
Melanaspis in North American (Homoptera: Diaspididae). No. 279.
Technical Bulletin North Carolina Agricultural Research Station, North
Carolina State University, Raleigh, NC.
Drea,J., and R.Gordon. 1990. Predators, pp. 19–98. In D.Rosen (ed.), World
crop pests. Armored scale insects: their biology, natural enemies and con-
trol, vol. 4B. Elsevier, Amsterdam, The Netherlands.
Ferris,G. 1941. Melanaspis tenebricosa (Comstock). In Atlas of the scale in-
sects of North America. Series 3. Stanford University Press, Stanford, CA.
Frank,S.D. 2012. Reduced risk insecticides to control scale insects and pro-
tect natural enemies in the production and maintenance of urban land-
scape plants. Environ. Entomol. 41: 377–386.
Frank,S.D. 2019. A survey of key arthropod pests on common southeastern
street trees. Arboric. Urban For. 45: 155–166.
Frank,S.D. 2020. Review of the direct and indirect effects of warming and
drought on scale insect pests of forest systems. Forestry. doi:10.1093/
forestry/cpaa033.
Frank,S., and A.Dale. 2015. Gloomy scale, Melanaspis tenebricosa (Comstock),
Hemiptera: Diaspididae. Entomology Insect Notes. NC State Cooperative
Extension, Raleigh, NC.
Frank,S. D., and M.G. Just. 2020. Can cities activate sleeper species and
predict future forest pests ? Acase study of scale insects. Insects 11: 142.
Frank, S. D., and J. F. Tooker. 2020. Opinion: Neonicotinoids pose un-
documented threats to food webs. Proc. Natl. Acad. Sci. USA 117:
22609–22613.
Frank,S. D., W. E. Klingeman, S.A.White, and A. Fulcher. 2013. Biology,
injury, and management of maple tree pests in nurseries and urban land-
scapes. J. Integr. Pest Manag. 4: 1–14.
Gan,H., and K.Wickings. 2017. Soil ecological responses to pest management
in golf turf vary with management intensity, pesticide identity, and applica-
tion program. Agric. Ecosyst. Environ. 246: 66–77.
García Morales, M., B. D. Denno, D.R. Miller, G. L. Miller, Y. Ben-Dov,
and N.B.Hardy. 2016. ScaleNet: a literature-based model of scale insect
biology and systematics. Database (Oxford) 2016: 1–5.
Greathead,D.J. 1972. Dispersal of the sugar-cane scale Aulacaspis tegalensis
(Zhnt.) (Hem., Diaspididae) by air currents. Bull. Entomol. Res. 61:
547–558.
Gullan,P.J., and M.Kosztarab. 1997. Adaptations in scale insects. Annu. Rev.
Entomol. 42: 23–50.
Hanks,L.M., and R.F.Denno. 1993a. The role of demic adaptation in colon-
ization and spread of scale insect populations, pp. 393–411. In K.Kim and
B.McPheron (eds.), Evolution of insect pests: patterns of variation. John
Wiley & Sons, Inc., New York.
Hanks,L.M., and R.F.Denno. 1993b. Natural enemies and plant water re-
lations inuence the distribution of an armored scale insect. Ecology 74:
1081–1091.
Herms,D.A., and W.Mattson. 1992. The dilemma of plants: to grow or de-
fend. Q. Rev. Biol. 67: 283–335.
Huberty,A.F., and R.F.Denno. 2004. Plant water stress and its consequences
for herbivorous insects: a new synthesis. Ecology 85: 1383–1398.
Hughes-Schrader,S. 1948. Cytology of Coccids (Coccoidea-Hornoptera). Adv.
Genet. 2: 127–203.
Johnson,W., and H.Lyon. 1976. Insects that feed on trees and shrubs. Cornell
University Press, London, United Kingdom.
Just, M. G., and S. D. Frank. 2020. Thermal tolerance of gloomy scale
(Hemiptera: Diaspididae) in the Eastern United States. Environ. Entomol.
49: 104–114.
Just,M.G., S.D.Frank, and A.G.Dale. 2018. Impervious surface thresholds
for urban tree site selection. Urban For. Urban Green. 34: 141–146.
Just,M.G., A.G.Dale, L.C.Long, and S.D.Frank. 2019. Urbanization drives
unique latitudinal patterns of insect herbivory and tree condition. Oikos
128: 984–993.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
Journal of Integrated Pest Management, 2020, Vol. 11, No. 1 9
Koricheva,J., S.Larsson, and E.Haukioja. 1998. Insect performance on ex-
perimentally stressed woody plants: a meta-analysis. Annu. Rev. Entomol.
43: 195–216.
Kosztarab, M. 1987. Everything unique or unusual about scale insects
(Homoptera: Coccoidae). Bull. Entomol. Soc. Am. 215–220.
Lahr,E.C., R.R.Dunn, and S.D.Frank. 2018. Variation in photosynthesis
and stomatal conductance among red maple (Acer rubrum) urban planted
cultivars and wildtype trees in the southeastern United States. PLoS One
13: e0197866.
Lahr,E. C., K. M. Backe, and S.D.Frank. 2020. Intraspecic variation in
morphology, physiology, and ecology of wildtype relative to horticultural
varieties of red maple (Acer rubrum). Trees Struct. Funct. 34: 603–614.
Larson,J. L., C. T.Redmond, and D.A. Potter. 2012. Comparative impact
of an anthranilic diamide and other insecticidal chemistries on benecial
invertebrates and ecosystem services in turfgrass. Pest Manag. Sci. 68:
740–748.
Larson,J.L., C. T.Redmond, and D.A. Potter. 2013. Assessing insecticide
hazard to bumble bees foraging on owering weeds in treated lawns. PLoS
One 8: e66375.
Lincango,B. P., C. Hodgson, C.Causton, and D.Miller. 2010. An updated
checklist of scale insects (Hemiptera: Coccoidea) of the Galapagos Islands,
Ecuador. Galapagos Res. 67: 3–7.
Long,L.C., V.D’Amico, and S.D.Frank. 2019. Urban forest fragments buffer
trees from warming and pests. Sci. Total Environ. 658: 1523–1530.
Luck, R., and D. Dahlstein. 1975. Natural decline of a pine needle scale
(Chionaspis pinifoliae [Fitch]), outbreak at South Lake Tahoe, California
following cessation of adult mosquito control with malathion. Ecology
56: 893–904.
Magsig-Castillo,J., J. G.Morse, G.P.Walker, J. L.Bi, P. F.Rugman-Jones,
and R. Stouthamer. 2010. Phoretic dispersal of armored scale crawlers
(Hemiptera: Diaspididae). J. Econ. Entomol. 103: 1172–1179.
McClure,M.S. 1977. Resurgence of the scale, Fiorinia externa (Homoptera:
Diaspididae), on hemlock following insecticide application. Environ.
Entomol. 6: 480–484.
McCullough,D.G., R.L. Heyd, and J.G.O’Brien. 2005. Biology and man-
agement of beech bark disease: Michigan’s newest exotic forest pest. No.
E-2746. Michigan State University Extension Bulletin, East Lansing, MI.
Metcalf, Z. 1912. The gloomy scale, an important enemy of shade trees in
North Carolina. J. Elisha Mitchell. Sci. Soc. 28: 88–91.
Metcalf,Z. 1922. The gloomy scale. North Carolina Agricultural Experiment
Station Technical Bulletin, Raleigh, NC.
Miller,D.R., and J.A.Davidson. 2006. Armored scale insect pests of trees and
shrubs. Cornell University Press, Ithaca, NY.
Parsons,S. E., K.S.Sozanski, A. A.Wilson, and S. D.Frank. 2020. Effects
of temperature and habitat complexity on an urban tree pest (Tinocallis
kahawaluokalani), natural enemies, and predation services in the city.
Urban Ecosyst. 23: 13–26.
Prado,J., C.Quesada, and C. Sadof. 2014. Effects of pesticide application
on arthropod pests of nursery-grown maples. J. Econ. Entomol. 107:
708–717.
Prado,J., C. Quesada, M.Gosney, M.V.Mickelbart, and C.Sadof. 2015a.
Effects of nitrogen fertilization on potato leafhopper (Hemiptera:
Cicadellidae) and maple spider mite (Acari: Tetranychidae) on nursery-
grown maples. J. Econ. Entomol. 108: 1221–1227.
Prado,J., A.R.Witte, S.Frank, and C.S.Sadof. 2015b. Do leaf domatia
mediate intraguild predation and host plant resistance to Oligonychus
aceris (Shimer) on red sunset maple (Acer rubrum)? Biol. Control 90:
187–192.
Quesada,C.R., and C. S. Sadof. 2017. Efcacy of horticultural oil and in-
secticidal soap against selected armored and soft scales. Horttechnology
27: 618–624.
Quesada,C.R., A.Witte, and C.S.Sadof. 2018. Factors inuencing insecticide
efcacy against armored and soft scales. Horttechnology 28: 267–275.
Quesada, C. R., M. E. Scharf, and C. S. Sadof. 2020. Excretion of non-
metabolized insecticides in honeydew of striped pine scale. Chemosphere
249: 126167.
Raupp,M.J., J.J.Holmes, C.Sadof, P.Shrewsbury, and J.A.Davidson. 2001.
Effects of cover sprays and residual pesticides on scale insects and natural
enemies in urban forests. J. Arboric. 27: 203–214.
Raupp,M. J., A.B. Cumming, and E.C. Raupp. 2006. Street tree diversity
in eastern North America and its potential for tree loss to exotic borers.
Arboric. Urban For. 32: 297–304.
Raupp,M.J., P.M.Shrewsbury, and D.A.Herms. 2010. Ecology of herbiv-
orous arthropods in urban landscapes. Annu. Rev. Entomol. 55: 19–38.
Raupp, M. J., P. M. Shrewsbury, and D.A. Herms. 2012. Disasters by de-
sign: outbreaks along urban gradients, pp. 313–340. In P. Barbosa,
D.Letourneau, and A.Agrawal (eds.), Insect outbreaks revisited. Blackwell
Publishing Ltd., Chichester, West Sussex, United Kingdom.
Rieske,L.K., S.Borden, B. Damron, N.I.C. Williamson, M.Arthur, and
A. Kinney. 2019. Scrubbing scales, saving trees, engaging students. Am.
Entomol. 65: 43–49.
Rolfs,P. 1897. A fungus disease of the San Jose scale. Bull. Fl. Agric. Exp. Stn.
41: 513–541.
Sadof,C. S., and D.C.Sclar. 2000. Effects of horticultural oil and foliar- or
soil-applied systematic insecticides on euonymus scale in pachysandra. J.
Arboric. 26: 120–125.
Santamour,F.S., and A. J.Mcardle. 1980. Check list of cultivated maples
I.Acer rubrum L. J. Aboricult. 8: 110–112.
Seagraves,B.L., C.T.Redmond, and D.A.Potter. 2013. Relative resistance
or susceptibility of maple (Acer) species, hybrids and cultivars to six
arthropod pests of production nurseries. Pest Manag. Sci. 69: 112–119.
Shrewsbury, P. M., and M. J. Raupp. 2000. Evaluation of components of
vegetational texture for predicting azalea lace bug, Stephanitis pyrioides
(Heteroptera: Tingidae), abundance in managed landscapes. Environ.
Entomol. 29: 919–926.
Speight,M.R., R.S.Hails, M.Gllbkrt, and A.Foggo. 1998. Horse chestnut
scale (Pulvinaria regalis) (Homoptera: Coccidae) and urban host tree en-
vironment. Ecology 79: 1503–1513.
Stoetzel,M.B. 1975. Seasonal history of seven species of armored scale insects
of the Aspidiotini (Homoptera: Diaspididae). Ann. Entomol. Soc. Am. 68:
489–492.
Strickland, A. H. 1950. The dispersal of pseudococcidae (Hemiptera-
Homoptera) by air currents in the gold coast. Proc. R.Entomol. Soc. Lond.
AGen. Entomol. 25: 1–9.
Szczepaniec,A., S.F.Creary, K.L.Laskowski, J.P.Nyrop, and M.J.Raupp.
2011. Neonicotinoid insecticide imidacloprid causes outbreaks of spider
mites on elm trees in urban landscapes. PLoS One 6.
Takagi, S., and H. Tippins. 1972. Two new species of the Diaspididae
occurring on Spanish moss in North America (Homoptera: Coccoidea).
Kontyu 40: 180–186.
Tooker,J. F., and L. M. Hanks. 2000. Inuence of plant community struc-
ture on natural enemies of pine needle scale (Homoptera: Diaspididae) in
urban landscapes. Environ. Entomol. 29: 1305–1311.
Townsend,A., and L.Douglass. 1998. Evaluation of various traits of 40 selec-
tions and cultivars of red maple and freeman maple growing in Maryland.
J. Environ. Hortic. 16: 189–194.
Waltman,K.G., C.H.Ray, and M.L.Williams. 2016. The armored scale in-
sects (Hemiptera diaspididae) of Alabama, USA. Redia 99: 229–231.
White,T.C.R. 1984. The abundance of invertebrate herbivores in relation to
the availability of nitrogen in stressed food plants. Oecologia 63: 90–105.
Xiao,Y., R.Mao, L.Singleton, and S.Arthurs. 2016. Evaluation of reduced-
risk insecticides for armored scales (Hemiptera: Diaspididae) infesting or-
namental plants. J. Agric. Urban Entomol. 32: 71–90.
Youngsteadt,E., A.G.Dale, A.J.Terando, R.R.Dunn, and S.D.Frank. 2015.
Do cities simulate climate change? Acomparison of herbivore response to
urban and global warming. Glob. Chang. Biol. 21: 97–105.
Downloaded from https://academic.oup.com/jipm/article/11/1/24/6047641 by guest on 15 January 2021
... Research is needed to understand the correlation between elevation and OSS infestation, but temperature is a likely explanation. Fitness and abundance of other scale insect pests has been linked to climate (Frank 2020;Just et al. 2020), and low temperatures are known to reduce survival of overwintering OSS eggs (Tothill 1919). Therefore, colder temperatures at higher elevations might directly limit OSS. ...
... On the other hand, a warmer climate may have directly improved conditions for OSS population growth by increasing the species' fitness and abundance (Frank 2020;Frank and Just 2020). Because OSS appears to be limited to aspen stands below 2500 m (Table 1), cold temperatures may be a limiting factor for its spread, which is consistent with other scale insect pests (Frank 2020;Just et al. 2020) and OSS in other locations (Furniss and Carolin 1977). Temperature changes that have already occurred may have enabled OSS's spread outside urban areas Just et al. 2020), and in the future, warmer temperatures at higher elevations and latitudes may promote further spread of OSS (Frank 2020). ...
... Because OSS appears to be limited to aspen stands below 2500 m (Table 1), cold temperatures may be a limiting factor for its spread, which is consistent with other scale insect pests (Frank 2020;Just et al. 2020) and OSS in other locations (Furniss and Carolin 1977). Temperature changes that have already occurred may have enabled OSS's spread outside urban areas Just et al. 2020), and in the future, warmer temperatures at higher elevations and latitudes may promote further spread of OSS (Frank 2020). The former would threaten the largest, healthiest aspen stands in northern Arizona, which occur at higher elevations, and the latter would threaten the rest of aspen's range in the western US because Arizona is situated on the southwestern edge of the tree's range. ...
Article
Full-text available
Oystershell scale (OSS; Lepidosaphes ulmi) is an emerging invasive insect that poses a serious threat to conservation of quaking aspen (Populus tremuloides) in the southwestern US. Although OSS has been an urban pest in the US since the 1700s, it has recently spread into natural aspen stands in northern Arizona, where outbreaks are causing dieback and mortality. We quantified the ongoing outbreak of OSS at two scales: (1) local severity at two sites and (2) regional distribution across northern Arizona. Our regional survey indicated that OSS is widespread in lower elevation aspen stands and is particularly pervasive in ungulate exclosures. Advanced regeneration had the highest levels of infestation and mortality, which is concerning because this size class is an underrepresented component of aspen stands in northern Arizona. If OSS continues to spread and outbreaks result in dieback and mortality like we observed, then aspen in the southwestern US, and perhaps beyond, will be threatened. Three interacting factors contribute to OSS’s potential as a high-impact invasive insect that could spread rapidly: (1) its hypothesized role as a sleeper species, (2) potential interactions between OSS and climate change, and (3) the species’ polyphagous nature. Invasive pests like OSS pose an imminent threat to native tree species and, therefore, represent an immediate research and monitoring priority. We conclude with recommendations for future research and monitoring in order to understand OSS’s biology in natural aspen stands, quantify impacts, limit future spread, and mitigate mortality and loss of aspen and other host species.
Article
Warmer temperatures and frequent drought directly affect urban tree health. Both abiotic conditions also affect tree health via increased density of some insect pests. Warming is predicted to benefit urban trees by increasing carbon sequestration and allocation to biomass. However, increased drought and pests are rarely considered despite often co-occurring with heat. To determine the combined effects of these abiotic and biotic factors, we manipulated water availability for established urban red maple trees across a gradient of warming and pest density and measured leaf-level processes and tree growth over two years. We find that water availability is a major determinant of tree growth, physiological processes, and resilience to urban stress factors. Maples performed better with more water, which also made them resistant to effects of temperature and pest density. However, when drought became too severe, leaf-level processes declined with warming. Tree basal area growth was unaffected after two years, but stem elongation increased with increasing water, temperature, and pest density. We discuss potential mechanisms driving these responses and the implications in the context of urban forest management. Urban forest designs that reduce drought and align species adaptations to local conditions are critical for designing more resilient and productive urban forests.
Article
Full-text available
The crapemyrtle bark scale is an invasive felt scale in the family Eriococcidae (or Acanthococcidae, as the taxonomy of this family is still being debated). This group is in the superfamily Coccoidea (scale insects) and the order Hemiptera (true bugs). Felt scales, also called bark scales, are not considered either armored scales or soft scales. As of early 2018, crapemyrtle bark scale has not yet been reported in Florida, however, it has been found in Alabama and Georgia and is expected eventually to spread into Florida. At that time, early detection and treatment will be critical to minimize further spread within the state. Includes: Introduction - Synonymy - Distribution - Description - Life Cycle and Biology - Hosts - Damage - Management - Selected References.https://edis.ifas.ufl.edu/in1218 Previously published at http://entnemdept.ufl.edu/creatures/ORN/SCALES/crapemyrtle_bark_scale.html
Article
Full-text available
The movement of invasive species is a global threat to ecosystems and economies. Scale insects are particularly well-suited to avoid detection, invade new habitats, and escape control efforts. In countries that celebrate Christmas, the annual movement of Christmas trees has in at least one instance been associated with the invasion of a scale insect pest and subsequent devastation of indigenous forest species. In the eastern United States, except for Florida, Fiorinia externa is a well-established exotic scale insect pest of keystone hemlock species and Fraser fir Christmas trees. Annually, several hundred thousand Fraser firs are harvested and shipped into Florida, USA for sale to homeowners and businesses. There is concern that this insect may disperse from Christmas trees and establish on Florida conifers of economic and conservation interest. Here, we investigate the invasive potential of F. externa on sixteen conifer species by quantifying the reproductive potential of this insect pest and its ability to establish, reproduce, and damage these plants. We find that small amounts of heavily infested Fraser fir plant material can release several hundred juvenile F. externa for over a month. Similar to other case studies, we find evidence that host susceptibility may in part be linked to phylogenetic relatedness. Encouragingly, only six of sixteen species evaluated were susceptible to attack. Our results provide new insights into methodology for evaluating scale insect dispersal and host susceptibility. We also provide guidance for future studies investigating scale insect reproduction, dispersal, and risk for plant species of unknown susceptibility to other exotic insect pests.
Article
Full-text available
Sleeper species are innocuous native or naturalized species that exhibit invasive characteristics and become pests in response to environmental change. Climate warming is expected to increase arthropod damage in forests, in part, by transforming innocuous herbivores into severe pests: awakening sleeper species. Urban areas are warmer than natural areas due to the urban heat island effect and so the trees and pests in cities already experience temperatures predicted to occur in 50-100 years. We posit that arthropod species that become pests of urban trees are those that benefit from warming and thus should be monitored as potential sleeper species in forests. We illustrate this with two case studies of scale insects that are important pests of urban trees in parts of the US. Melanaspis tenebricosa and Parthenolecanium quercifex are geographically native to the US but take on invasive characteristics such as higher survival and reproduction and become disconnected from natural enemies on urban trees due to the urban heat island effect. This allows them to reach high densities and damage their host trees. Parthenolecanium quercifex density increases up to 12 times on urban willow oaks with just 2 °C of warming due to higher survival and adaptation to warmer temperatures. The urban heat island effect also creates a phenological mismatch between P. quercifex and its parasitoid complex, and so egg production is higher. Melanaspis tenebricosa density can increase 300 times on urban red maples with 2.5 °C of warming. This too is due to direct effects of warmer temperatures on survival and fecundity but M. tenebricosa also benefits from the drought stress incurred by warmer urban trees. These effects combine to increase M. tenebricosa density in forests as well as on urban trees at latitudes higher than its native range. We illustrate how cities provide a unique opportunity to study the complex effects of warming on insect herbivores. Studying pestilent urban species could be a pragmatic approach for identifying and preparing for sleeper species.
Article
Full-text available
Honeydew production is a characteristic of soft scales and other hemipteran insects. Honeydew has the capacity to alter the ecology of predators and parasitoids because it is used as a food resource and can contain insecticidal proteins from hemipteran host plants. We examined honeydew excreted by the striped pine scale (Hemiptera: Coccidae), Toumeyella pini (King), after feeding on pine trees treated with systemic insecticides to determine whether they could eliminate insecticidal compounds in honeydew. Imidacloprid and spirotetramat were applied at labeled rates to soil or foliage. Water sensitive paper was used to measure honeydew production and liquid chromatography coupled to mass spectrometry (LC-MS) to analyze excreted insecticide concentrations. Foliar and soil applications of imidacloprid caused a 25-fold reduction honeydew produced by scales six days after treatment (DAT). In contrast, spirotetramat treatments did not affect honeydew production. Parent compounds of both insecticides were detected in honeydew. However, on imidacloprid treated plants, these compounds were detected at similar concentrations in honeydew collected at 4 DAT from soil and foliar treatments. Imidacloprid was only detected from soil treatments at 8 DAT. Similarly, the spirotetramat parent compound was found 4 DAT after soil and foliar treatments, but only at 8 DAT in foliar treatments. At this time the concentration of spirotetramat in honeydew was six-fold higher than at 4 DAT. We conclude that striped pine scales excrete insecticides in honeydew even when the toxicant greatly reduces honeydew production. Honeydew excretion is thus a mechanism of bioaccumulation and has the potential to harm honeydew-feeding organisms.
Article
Cities contain dozens of street tree species each with multiple arthropod pests. Developing and implementing integrated pest management (IPM) tactics, such as scouting protocols and thresholds, for all of them is untenable. A survey of university research and extension personnel and tree care professionals was conducted as a first step in identifying key pests of common street tree genera in the Southern United States. The survey allowed respondents to rate seven pest groups from 0 (not pests) to 3 (very important or damaging) for each of ten tree genera. The categories were sucking insects on bark, sucking insects on leaves, defoliators and leafminers, leaf and stem gall forming arthropods, trunk and twig borers and bark beetles, and mites. Respondents could also identify important pest species within categories. Some tree genera, like Quercus and Acer, have many important pests in multiple categories. Other genera like Liriodendron, Platanus, and Lagerstroemia have only one or two key pests. Bark sucking insects were the highest ranked pests of Acer spp. Defoliators, primarily caterpillars, were ranked highest on Quercus spp. followed closely by leaf and stem gallers, leaf suckers, and bark suckers. All pest groups were rated below ‘1’ on Zelkova spp. Identifying key pests on key tree genera could help researchers prioritize IPM development and help tree care professionals prioritize their training and IPM implementation. Recommendations for future surveys include having more respondents and tree taxa represented and identifying trees to species within large genera, such as Acer and Quercus.
Article
Higher temperatures and drought are key aspects of global change with the potential to alter the distribution and severity of many arthropod pests in forest systems. Scale insects (Hemiptera: Coccoidea) infest many tree species and are among the most important pests of trees in urban and rural forests, plantations and other forest systems. Infestations of native or exotic scale insects can kill or sicken trees with economic and ecosystem-wide consequences. Warming can have direct effects on the life history, fitness and population dynamics of many scale insect species by increasing development rate, survival or fecundity. These direct benefits can increase the geographic distribution of scale insects and their consequences for tree health. Warming and drought can affect scale insects indirectly by altering the quality of their host trees. Additive or interactive effects of warming and drought can change tree quality in such a way that it increases scale insect fitness and population growth. However, the effects are species- and context-dependent with some scale insect species negatively affected by drought-induced changes in tree quality. Warming and drought are often coincident in urban forests and predicted to co-occur in many parts of the world under climate change scenarios. The individual and interactive effects of these factors require further research to inform predictions and management of scale insect pests. Warming also indirectly affects scale insects by altering interactions with natural enemies. This includes changes in natural enemy phenology, community composition and abundance. In addition, warming can alter scale insect phenology or voltinism causing asynchrony with natural enemies or population growth too rapid for natural enemies to suppress. Direct and indirect effects of warming and drought on scale insects can increase the potential for some exotic species to become established and for some native species to become invasive. Unfortunately, much research on scale insects is confined to a few particularly important native or exotic pests which limits our ability to predict the effects of warming on many current or potential pests. More research is required to understand how warming and drought affect scale insects, scale insect management and the forest systems they inhabit.
Article
Thirty-seven red maple (Acer rubrum L.) and three Freeman maple (A. x freemanii E. Murray) selections and commercial cultivars were evaluated for six years in a replicated field plot at Glenn Dale, MD. Significant differences among clones occurred for growth rate; for time, intensity, and duration of autumn color; for time of growth initiation in the spring; and for injury sustained from potato leafhopper (PLH) [Empoasca fabae (Harris)] feeding. The red maple cultivars showing the best red color over three years time were ‘Autumn Flame,’ ‘Brandywine,’ ‘Cumberland,’ ‘Red Rocket,’ ‘Somerset,’ ‘Sun Valley,’ and ‘Van.’ The cultivar ‘Bowhall’ was the least reddish. Of the three Freeman maples evaluated, ‘ Jeffersred’ and ‘Indian Summer’ manifested the best red color and also low PLH injury; whereas ‘Armstrong’ consistently showed the least reddish color of all 40 clones tested, and intermediate PLH injury. Those cultivars and selections from northern seed sources reached their peak color the earliest, but often dropped their leaves more quickly after showing their best color, compared to clones originating in more southerly locations. The clones showing the least PLH injury over several years included the Freeman maples ‘Jeffersred’ and ‘Indian Summer,’ and red maple clones and cultivars selected by the U.S. National Arboretum either from full-sib progenies (e.g., ‘Brandywine,’ ‘Somerset,’ ‘Sun Valley’) or from an Ohio provenance-progeny test (e.g., ‘Cumberland,’ ‘Red Rocket’). Those clones initiating growth (or “flushing”) earliest in the spring generally showed the least PLH injury; correlations between lateness of flushing and degree of PLH injury were highly significant.
Article
An insect species' geographic distribution is probably delimited in part by physiological tolerances of environmental temperatures. Gloomy scale (Melanaspis tenebricosa (Comstock)) is a native insect herbivore in eastern U.S. forests. In eastern U.S. cities, where temperatures are warmer than nearby natural areas, M. tenebricosa is a primary pest of red maple (Acer rubrum L.; Sapindales: Sapindaceae) With warming, M. tenebricosa may spread to new cities or become pestilent in forests. To better understand current and future M. tenebricosa distribution boundaries, we examined M. tenebricosa thermal tolerance under laboratory conditions. We selected five hot and five cold experimental temperatures representative of locations in the known M. tenebricosa distribution. We built models to predict scale mortality based on duration of exposure to warm or cold experimental temperatures. We then used these models to estimate upper and lower lethal durations, i.e., temperature exposure durations that result in 50% mortality. We tested the thermal tolerance for M. tenebricosa populations from northern, mid, and southern locations of the species' known distribution. Scales were more heat and cold tolerant of temperatures representative of the midlatitudes of their distribution where their densities are the greatest. Moreover, the scale population from the northern distribution boundary could tolerate cold temperatures from the northern boundary for twice as long as the population collected near the southern boundary. Our results suggest that as the climate warms the M. tenebricosa distribution may expand poleward, but experience a contraction at its southern boundary.