Abstract
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.
INTRODUCTION
Integrated pest management (IPM) for urban trees has been studied for decades (Olkowski et al. 1974). Yet key IPM components developed for agricultural systems, such as standard scouting and monitoring practices, decision making criteria, and cultural management tactics, are not well developed for urban trees (Raupp et al. 1992; Fettig et al. 2005; Raupp et al. 2010; Frank et al. 2013). A major difference between IPM for urban trees compared to agricultural crops is the diversity of plant and pest species and the complexities of the landscape. For example, cities may have dozens of street tree genera and hundreds of species (Raupp et al. 2006). Each tree species hosts many specialist and generalist herbivorous arthropod species (Nielsen et al. 1985; Frank et al. 2013). Even if each species has just one to three key pests (Raupp et al. 1985), the number of pests for which monitoring (e.g., degree day models, traps) and decision-making tools (e.g., economic injury or action thresholds) are needed is immense.
The diversity of urban tree species and their arthropod pests necessitates development of clear IPM priorities to help researchers focus limited resources on the most common or damaging pests or those that require the most pesticide applications. A first step toward developing research priorities is identifying the key pests associated with common urban tree taxa. Key pests are those that frequently or persistently cause severe damage and account for a disproportionate amount of control effort or expense (Smith and Van den Bosch 1967). Focusing on the key pests of common, key plants—those that sustain disproportionately more pests or damage—can increase the efficiency of developing and implementing IPM programs (Raupp et al. 1985; Raupp et al. 2001).
University research and extension personnel, and others in the tree care industry, were surveyed to identify key arthropod pests of the most common genera of street trees in the Southeastern U.S.A. There have been several attempts to rank the importance of arthropod pest species of urban trees based on prevalence, economic cost, and pesticide use (Kielbaso and Kennedy 1983; Neely et al. 1984; Nielsen et al. 1985; Wu et al. 1991). However, none have been conducted in the past 30 years, during which time new exotic pests have arrived, preference for tree species has changed, and atmospheric temperature has increased. For example, the USDA updated the Plant Hardiness zones to reflect higher average winter temperatures across the U.S.A. (USDA 2012). Thus, the geographic range within which some tree species may be suitable has changed along with the distribution of some pests.
Review of Previous Pest and IPM Assessments
One of the first assessments of pest status on urban trees is from Kielbaso and Kennedy (1983). In 1980, they surveyed 1534 municipal tree care professionals, then ranked the pests by region in the Northeast, North Central, South, West, and Nationally. In 1991, Wu et al. (1991) reported a comparison between the 1980 survey and a new, similar survey in 1986 of 1062 municipalities. Respondents were asked to list the tree pests they considered most important. Rankings varied by region as in the previous assessment by Kielbaso and Kennedy (1983). In the South, borers, bagworms, and aphids were the top three pests, followed by webworms and scales. Pine bark beetle is reported on the Southern list, which was not reported in other regions. Nielsen et al. (1985) conducted a survey of 44 communities in the North Central region about the common street tree species and pest problems.
These surveys provide the relative importance of pests in each region, but their interpretation is limited by two factors. Respondents were free to list taxa based on their experience or expertise rather than selecting from a list of choices. Respondents listed 81 arthropod taxa, an indication of the diversity of tree pests, but the taxonomic specificity varied, and not all taxa were reported to species (Wu et al. 1991). For example, in Wu et al. (1991), many lepidopterans are listed, some of which are species (e.g., gypsy moth), while others are colloquial designations (e.g., webworms, tent caterpillars) in addition to just “caterpillar.” Lepidopteran larvae are large, cause noticeable damage and frass, and are easy to identify, so a list of “top ten” pests may be populated with several types of caterpillar. However, cryptic taxa show up in the surveys as just “scales” or “borers” and may be ranked lower as a result. In addition, previous surveys did not ask respondents to match important pests to the tree taxa on which they occurred. Thus, rankings are driven in part by particularly abundant or pest-prone tree species. Although this provides an important picture of what managers were dealing with on a city-wide basis, it does not help identify which tree taxa are most pest-prone and which taxa with fewer pests may be alternatives.
METHODS
Street tree genera and pests differ throughout the country (Wu et al. 1991). A particularly important factor affecting tree selection and pest abundance is climate, which varies with latitude. Therefore, this survey focused on arthropod pests of street trees in the Southern U.S.A., since the goal was to identify current key pests in one region and compare to past assessments, rather than compare among regions. The region included Alabama, Arkansas, Florida, Georgia, Kentucky, Louisiana, Mississippi, North Carolina, Oklahoma, South Carolina, Tennessee, Texas, and Virginia, following the definition of the “Southern Region” used by the USDA Southern IPM Center.
The survey was distributed via national email listservs that include university research and extension faculty and professionals involved in the tree care industry, such as those who work for municipalities, tree care companies, industry organizations, and agrochemical companies. The initial request for participation was sent on March 3, 2017 and described the focus and goals of the survey. Those who were willing to participate then received the survey, along with specific individuals who were invited to increase participation and industry representation.
Twelve tree genera were included in the survey that are commonly planted as street trees in the Southeastern U.S.A.: Acer, Fraxinus, Lagerstroemia, Liquidambar, Liriodendron, Pinus, Platanus, Prunus, Pyrus, Quercus, Ulmus, and Zelkova. These genera were selected because they were represented by the most individual trees listed in tree inventories from five Southeastern cities: Atlanta, GA; Savannah, GA; Charleston, SC; Charlotte, NC; and Raleigh, NC (Just et al. 2018).
Previous pest assessment surveys have used many different taxonomic groups and ranking systems. This survey focused on broad pest categories but also sought information on specific pest species that are most prevalent or problematic within those categories. Seven broad pest categories were created based on feeding guild and damage caused. Pest 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 completed two tables in the survey. The first had a row for each of the twelve tree genera and a column for each pest category. Respondents recorded a value of 3 (very common/damaging), 2 (moderate), 1 (rare/not very damaging), or 0 (not a pest) in each cell of the first table based on their expertise and experience with trees in the Southeastern U.S.A. Values were presented as “very common/damaging” and “rare/not very damaging,” since it is possible for pests to be common in the environment but cause minor or infrequent damage, and for pests to be relatively rare but very damaging when they do occur. Each respondent could balance their perception of commonness and severity to select a score. A mean was calculated for each tree/pest combination recorded (Table 1).
In the second table, respondents listed the most important pest species for each tree genus from the pest category they considered to be most important from the first table. For example, if a respondent considered “leaf suckers” to be the most important category of pests on Acer spp. in the first table, they would list the species of “leaf suckers” they thought were important in the second table. Since the same pest category was not always selected by all respondents, these data are presented in Table 2 as the pest category with the highest mean in the first table followed by the pest species listed by respondents as important in that category. In addition, the survey presents the pest species listed by respondents who considered other pest categories most important (Table 2).
RESULTS AND DISCUSSION
15 completed surveys were received from people residing in the following eight Southeastern states: Alabama (1), Florida (2), Kentucky (2), North Carolina (4), Oklahoma (1), South Carolina (1), Tennessee (3), and Virginia (1). Respondents included 12 university research or extension faculty, two technical specialists at tree care firms, and one city forester.
Sucking Insects on Bark
This category primarily includes scale insect species, in particular armored scales. Pests in this category feed on fluid in phloem, parenchyma, cambium, or other vascular tissues, and damage trees by reducing the energy available for growth and storage. Infested trees may have slowed growth, sparse canopies, and dead branches. Over 100 years ago, Metcalf identified gloomy scale (Melanaspis tenebricosa) as the most important shade tree pest in North Carolina (Metcalf 1912; Metcalf 1922). Scale insects (family not specified) remained important pests in 1980, ranked third in importance in the Southern U.S.A. and 2nd nationally (Kielbaso and Kennedy 1983). A survey in 1986 found scales ranked fifth in the South behind two caterpillar species, aphids, and borers. Scales were also among the top pests in two surveys of urban landscapes (not only trees) (Holmes and Davidson 1984; Raupp and Noland 1984) and trees in the North Central U.S.A. (Nielsen et al. 1985; Kielbaso and Kennedy 1983).
In most assessments, scales have ranked in the top five pests of trees. Currently, bark feeding scales are especially important pests of Acer spp. Gloomy scale was the most frequently listed species. Eight other armored and soft scale species were also identified as important. Bark sucker scales ranked second on Liriodendron spp. and included just one species: Tuliptree scale (Toumeyella liriodendri). This is in contrast with Quercus spp. on which bark suckers ranked fourth behind defoliators, gallers, and leaf suckers, but with a higher mean rating (1.73) than Liriodendron spp., and with five scale taxa listed as important by respondents. Comparing results for Quercus spp. and Liriodendron spp. highlights that a pest, like scales, can rank highly on a tree taxa with few pests, like Liriodendron spp., whereas scales rank lower on Quercus spp. but are more diverse and considered more important.
This survey captured a new pest, crape myrtle bark scale (Acanthococcus lagerstroemiae), which is in the process of spreading across the South. Respondents from areas already invaded by crape myrtle bark scale identified bark suckers as most important, but respondents in uninvaded areas identified leaf suckers, of which crape myrtle aphid (Tinocallis kahawaluokalani) is the only species, as most important. Crape myrtle bark scale is a more damaging pest than crape myrtle aphid and more difficult to manage. A survey conducted several years from now would likely document crape myrtle bark scale to be most important throughout the region.
Sucking Insects on Leaves
Primary pests in this category include phloem-feeding scales, aphids, and whiteflies. Phloem feeders damage trees by removing carbon and nutrients needed for growth and storage and can reduce photosynthesis and other leaf processes. In addition, phloem feeders excrete a sticky sugar-based solution called honeydew that coats leaves, cars, sidewalks, and other surfaces. This creates a nuisance and is often the subject of citizen complaints. For this reason, previous pest assessments often have ranked soft scales and aphids, such as elm aphids and oak aphids, in the top five pests of every region in the United States (Kielbaso and Kennedy 1983; Nielsen et al. 1985; Wu et al. 1991).
Leaf suckers were the top ranked pest for Liriodendron spp., Lagerstroemia spp., and Platanus spp. in this survey. Tuliptree aphids (Illinoia liriodendri) can become very abundant on tulip trees where they produce copious honeydew and cause leaves to become discolored or die (Dreistadt and Dahlsten 1988). The density of honeydew drops landing below a tree can be used to monitor tuliptree aphid density as part of an IPM program (Dreistadt 1987). The most important pest of Platanus spp. is sycamore lace bug (Corythucha ciliata) a leaf sucker that causes extensive stippling on leaves which then become discolored or die. This was the only arthropod pest identified as important on Platanus spp. in this survey, though Platanus spp. are susceptible to other arthropod pests and leaf pathogens, such as leaf scorch (Xylella fastidiosa) and plane anthracnose (Apiognomonia veneta)(Filer 1977).
Leaf suckers were ranked third for Quercus spp. yet rated highly in importance (1.93). Several leaf sucking insects occur on Quercus spp., including oak lace bugs (Corythucha arcuata) and aphids (Johnson and Lyon 1976). The most prominent in the South and identified most in the survey are Parthenolecanium spp. Scales, including oak lecanium scale (P. quercifex), and European fruit lecanium scale (P. corni). These scales can become very abundant on willow oaks and other Quercus spp., especially under urban conditions (Meineke et al. 2013; Meineke and Frank 2018). They are univoltine throughout the South, and their life cycle includes leaf feeding and bark feeding stages (Camacho et al. 2017). This identifies a weakness in the pest categories used for the survey, because some respondents listed Parthenolecanium spp. as bark suckers and others listed them as leaf suckers. Since Parthenolecanium spp. scales were the primary pest listed in both categories, scales likely would rank higher as pests of Quercus spp. if responses were combined in a more specific category.
Defoliators and Leafminers
Caterpillars are important pests of some tree species. They can defoliate susceptible species, and repeated defoliation can reduce tree growth and survival (Kulman 1971; Coffelt et al. 1993). Even partial defoliation can reduce tree growth and beauty and provoke citizen complaints (Coffelt and Schultz 1990). Caterpillar frass can be a nuisance accumulating on sidewalks, decks, cars, and other surfaces, causing citizen complaints (Coffelt and Schultz 1990). Previous pest assessments have listed lepidopteran defoliators as a top pest during outbreaks of exotic pests like gypsy moth and native pests like orange-stripped oakworms and cankerworms (Nielsen et al. 1985; Wu et al. 1991; Kielbaso and Kennedy 1983). Since lepidopteran species often have outbreak cycles of many years, they may not be important pests every year.
In this survey, lepidopteran defoliators were most important on Prunus spp. (2.27) due primarily to Prunus spp. susceptibility to eastern tent caterpillar (Malacosoma americanum), which prefer Prunus spp. such as black cherry (Prunus serotina) and can defoliate trees. Spring cankerworm (Paleacrata vernata) and fall cankerworm (Alsophila pometaria) are generalist caterpillars that feed heavily on many tree taxa including Prunus spp. Defoliators including cankerworms and more specialized caterpillars, such as orange-striped oakworm (Anisota senatoria), were the highest rated pests on Quercus spp. Orange-striped oakworms and cankerworms can defoliate large expanses of urban areas garnering citizen complaints, harming trees, and often leading to expensive management practices (Coffelt et al. 1993; Chanthammavong et al. 2014; Asaro and Chamberlin 2015).
Beetles eat tree leaves as larvae, adults, or both depending on species. Coleopteran defoliators, like Japanese beetles (Popillia japonica), imported willow leaf beetles (Plagiodera versicolora), and elm leaf beetles (Xanthogaleruca luteola), can be severe pests on certain tree species. In the 1980s, elm leaf beetle was among the highest ranked tree pest nationally but was ranked lower in the South (Wu et al. 1991). Elms are less common now due to Dutch elm disease, but new resistant American elm genotypes and Asian species such as Siberian elm (U. pumila) and lacebark elms (U. parvifolia) are becoming more common in urban plantings. Although elm leaf beetle was identified as an important elm pest in this survey, recent research suggests European elm flea weevil (Orchestes alni) is the most frequent beetle to damage elm leaves in many regions (Condra et al. 2010; Griffin and Jacobi 2016). European elm flea weevil was first discovered in North America in 2007 and has since become widespread (Anderson et al. 2007). European elm flea weevil larvae mine leaves, whereas elm leaf beetle larvae skeletonize leaves. Determination of which pest species is present will inform the best course of management.
Sawflies can be important defoliators, primarily of evergreen tree species, that reduce tree growth and survival (Kulman 1971). Only one sawfly species, Redheaded pine sawfly (Neodiprion lecontei), was identified as a pest in this survey.
Leaf and Stem Gallers
Galls, such as horned oak gall (Callirhytis cornigera), become important pests in some situations (Johnson and Lyon 1976). Galls have not been ranked highly or even appeared in previous pest assessments. However, their consequences for plant vigor and management can be severe (Eliason and Potter 2000a; 2000b; 2001). Quercus spp. appear to have the most consequential gall pests of the tree genera in this survey. Gallers were essentially tied with defoliators as the most important pest category of Quercus spp., with horned oak gall and gouty oak gall (Callirhytis quercuspunctata) mentioned most frequently.
Trunk and Twig Borers
Important trunk boring insects are primarily coleopteran and lepidopteran species. Borers are often difficult to control, and the consequences of borer attacks can be rapid and severe. Thus, borers have ranked highly in previous pest assessments. For example, “borers”’ ranked as the first and third most important street tree pest in the Southern and North Central U.S.A. and fourth nationally (Kielbaso and Kennedy 1983; Wu et al. 1991). Several exotic borers that are devastating pests have arrived since these surveys were conducted, including emerald ash borer (Agrilus planipennis), Asian longhorned borer (Anoplophora glabripennis), and walnut twig beetle (Pityophthorus juglandis).
Borers were the most important pest category of Fraxinus spp. due to emerald ash borer, which is spreading through the South. Borers of Pinus spp. are primarily Scolytine beetles. The most serious pest of Pinus spp. is southern pine beetle (Dendroctonus frontalis), which attack trees en masse, especially when trees are stressed by drought or injury. Southern pine beetle is an example of how the importance of pests can change due to higher temperatures, as it has spread north as far as Massachusetts where it did not occur before the last decade (Dodds et al. 2018). In the south, flat-headed apple tree borer (Chrysobothris femorata) and ambrosia beetles, such as Xylosandrus crassiusculus, are pests of some tree species especially when stressed by drought, flooding, winter damage, or injury (Frank and Ranger 2016; Ranger et al. 2016; Frank et al. 2017).
Mites
Spider mites can be important pests of some urban tree species. Spider mite abundance can erupt in response to environmental conditions such as impervious surface cover, heat, drought, or dust (Ehler and Frankie 1979; Rigamonti and Lozzia 1997; Sperry et al. 2001; Kropczynska et al. 2002; Meineke et al. 2016), or in response to anthropogenic inputs such as insecticides (Szczepaniec et al. 2011), fertilizer (Prado et al. 2015), or road salts (Fostad and Pedersen 1997). Thus, they are often innocuous until some environmental conditions or disturbance occur. Due to their sporadic outbreaks, mites are not always ranked highly in urban tree pest assessments (Kielbaso and Kennedy 1983; Wu et al. 1991). However, spider mites were among the most common and problematic pests in urban landscapes and among the pests for which the most pesticide applications were made (Holmes and Davidson 1984; Raupp and Noland 1984; Braman et al. 1998). Mites were not the highest ranked pests of any tree genera in this survey. Mites ranked highest on Acer spp. and Quercus spp., which can be infested with maple spider mites (Oligonychus aceris) and oak spider mites (O. bicolor). These can become abundant after insecticide applications that kill natural enemies and due to excess nitrogen that improves leaf quality (Frank and Sadof 2011; Prado et al. 2015).
DISCUSSION
Overall, Quercus spp. has the highest total pest rating, which is the mean of all seven pest categories, and Acer spp. has the second highest. This does not mean that Quercus spp. or Acer spp. are necessarily more pest prone or poorer choices for planting along streets or in landscapes. Considering trees at the genus level means some genera, such as Quercus and Acer, are each represented by dozens of species, but genera such as Liriodendron, Platanus, and Zelkova are each represented by one. Thus, when respondents consider all the species in a large genus, it is likely they can think of a species on which bark sucking insects are important, a species on which leaf sucking insects are important, and another on which defoliators are important. A genus with one or two species could seem relatively pest free by comparison.
The provenance of trees is another important consideration when interpreting the total pest score for each genus. Zelkova spp. is represented primarily by a single species, Z. serrata, imported from Asia. Exotic trees often host fewer herbivore species, at least initially, than native trees (Southwood 1961; Burghardt and Tallamy 2013). Quercus and Acer, for example, are represented primarily by native species that may host hundreds of herbivore species (Southwood 1961; Tallamy and Shropshire 2009). A few of these herbivores, such as scales or caterpillars, may become pests under urban conditions (Coffelt et al. 1993; Meineke et al. 2013; Dale and Frank 2014; Dale and Frank 2018). Quercus and Acer also contain exotic species with few pests, such as sawtooth oak (Quercus acutissima), trident maple (Acer buergerianum), and Norway maple (Acer platanoides).
Key plants in an IPM program are those that have a disproportionate amount of pests or damage or those that are particularly valuable (Raupp et al. 1985). In this sense, some native Quercus spp. and Acer spp. may constitute key plants that are more pest prone than other species. Consumers and municipalities often have goals of increasing the number of native species planted as a conservation measure to preserve arthropod and bird populations. Greater use of native species combined with their higher herbivore abundance suggests that researchers and practitioners should prioritize developing IPM tactics for the most common and pest prone native trees. From the inventories used in the survey, these include species such as Q. phellos, Q. palustris, Q. falcata, and A. rubrum. A more detailed survey of species within these genera would be required to ascertain key plants on which to focus research and management. A future survey should also include susceptibility to abiotic conditions and pathogens.
Key pests are those that frequently or persistently cause severe damage and account for a disproportionate amount of control effort or expense (Smith and Van den Bosch 1967). Galling arthropods and mites appear to be the least important pest categories among the tree genera in this survey. Pests in both of these categories can be very destructive on some tree species under certain conditions and can be more difficult to manage due to concealed or cryptic life stages and fewer available pesticides (Kropczynska et al. 1988; Eliason and Potter 2000b; Eliason and Potter 2001; Szczepaniec et al. 2011). Thus, galling insects or mites may constitute key pests for some arborists. The other four pest categories have similar ratings, though leaf sucking insects is highest. Most tree genera had leaf feeding scales, aphids, or lace bugs identified as important in the survey. These and bark sucking insects qualify as key pests on susceptible species due to their persistence and density. Phloem feeding insects in this group have the added problem of producing honeydew (Dreistadt and Dahlsten 1988).
Defoliators were also important overall. As key pests, they are often sporadic rather than persistent, but are very damaging to their hosts and adjacent plants with damage and frass that is apparent to the public (Schultz and Sivyer 2006; Eirich 2008; Frank 2014). This leads to high demand for expensive management practices when defoliator outbreaks occur (Coffelt and Schultz 1990; Eirich 2008). Similarly, borers may occur sporadically but with severe consequences, such as rapid tree death. The importance of this will depend largely on the number of susceptible trees (Raupp et al. 2006). For example, emerald ash borer is a key pest that is devastating municipalities in Northern and Central states that have a high proportion of ash trees. In Southern regions, where ash trees are less common, the effect of emerald ash borer on individual trees is still severe, but consequences for municipalities are less. The prominence of Pinus spp. increases the risk from southern pine beetles.
The diversity of plants and pests in urban landscapes makes IPM education and implementation difficult. This survey provides an overview of the most important pest categories on the most common tree genera in the Southern U.S.A. Assessing pest risk by plant genera has proven valuable in previous research (Raupp and Noland 1984; Raupp et al. 1985; Raupp et al. 2006). This survey provides insight into the trees and pests on which research, extension, and industry personnel could focus IPM development and implementation efforts. It also provides information to improve future surveys, for example, by focusing on species of prominent genera such as Quercus and Acer and by not including genera with few species or few pests such as Zelkova, Lagerstroemia, and Liriodendron. Some respondents suggested adding genera including Magnolia, Cornus, Cercis, and Cupressus to future surveys. A future survey would also benefit from including tree pathogens and by including more respondents, especially more respondents employed as arborists and municipal foresters. A direct benefit of this research for arborists and municipal foresters is helping to focus formal and individual education efforts. Identifying important pest categories and species will help extension educators focus their teaching and practitioners focus their learning on pests likely to be key in their situations.
ACKNOWLEDGEMENTS
The author thanks the survey respondents for their time and effort, which made this work possible. Michael Just and the survey respondents provided comments on previous versions of this manuscript. Components of referenced and ongoing work by Dr. Steven D. Frank have been supported by the United States Department of Agriculture National Institute of Food and Agriculture funded Southern IPM Center, under Agreement No. 2014-70006-22485, as well USDA NIFA award numbers 2013-02476 and 2016-70006-25827 to Dr. Frank. The project described in this publication was also supported by Cooperative Agreement no. G15AP00153 from the United States Geological Survey. Its contents are solely the responsibility of the author and do not necessarily represent the views of the Southeast Climate Science Center or the USGS. This manuscript is submitted for publication with the understanding that the United States Government is authorized to reproduce and distribute reprints for governmental purposes.
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