POPULATION ECOLOGY

Inuence of Plant Community Structure on Natural Enemies of Pine Needle Scale (Homoptera: Diaspididae) in Urban Landscapes
JOHN F. TOOKER
AND

LAWRENCE M. HANKS

Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801

ABSTRACT Pine needle scale, Chionaspis pinifoliae (Fitch), is a pest of many species of conifers in urban habitats and Christmas tree farms. We found that the scale was abundant in impoverished habitats, such as ornamental landscapes, and scarce in more natural, park-like habitats. Rates of parasitism were highest in impoverished habitats, suggesting that parasitoids were not effective in suppressing scale populations. Generalist predators, however, were more diverse and abundant in natural habitats and appear to be more effective in controlling scales in structurally complex plant communities. Total densities of arthropods and densities of plant-feeding species were greatest in impoverished habitats, suggesting that populations were poorly regulated. Outbreaks of pine needle scale in ornamental landscapes and Christmas tree farms may be discouraged by increasing plant structural and species diversity to favor natural enemies. KEY WORDS Aphelinidae, Aphytis, Chionaspis heterophyllae, habitat effects, natural enemies, conservation biological control

Environ. Entomol. 29(6): 13051311 (2000)

IN BOTH NATURAL and managed ecosystems, species diversity of arthropod natural enemies is often positively correlated with the diversity of plant species (e.g., Risch 1981, Yue et al. 1994, Dean and Milton 1995). Plants sustain populations of natural enemies by providing prey, oral resources for adults, and suitable microclimates (Powell 1986, van Emden 1990). Thus, diversifying the composition of plant communities could encourage natural enemies to suppress populations of phytophagous insects. Ornamental landscapes are amenable to this pest management tactic because they are relatively stable ecosystems and are not constrained by the simple structure and periodic disruption characteristic of agronomic systems (Raupp et al. 1992). Diverse and structurally complex plant communities in ornamental landscapes support a higher diversity and abundance of natural enemies, resulting in better regulation of phytophagous insects (e.g., Hanks and Denno 1993, Shrewsbury 1996). We examined the inuence of plant community structure of urban landscapes on the abundance and diversity of natural enemies, and, indirectly, on population densities of pine needle scale, Chionaspis pinifoliae (Fitch). Pine needle scale is native to North America (Burden and Hart 1989), but is a serious pest of many species of introduced evergreens, including species in the Pinaceae (Abies, Picea, Pinus, Pseudotsuga, and Tsuga), Cupressaceae (Juniperus), and Taxaceae (Taxus, Torreya; Shour and Schuder 1987). The scale is one of the most important pests of ornamental pines in the United States, and has been labeled the white malady because heavily infested trees appear whitewashed (Johnson and Lyon 1988).

Damaging infestations of pine needle scale are usually limited to managed ecosystems, such as nurseries, tree farms, and ornamental landscapes (Johnson and Lyon 1988) that are often characterized by low levels of plant species diversity and structural complexity (Raupp et al. 1992). The scale is rare in more natural habitats, such as forests and wood lots (Ruggles 1931) where complexity and plant diversity are higher (see Risch 1981, Szentkiralyi and Kozar 1991, Yue et al. 1994, Dean and Milton 1995). Natural enemies of pine needle scale include coccinellid beetles (Cumming 1953, Nielsen and Johnson 1973, Luck and Dahlsten 1974, Eliason and McCullough 1997) and at least nine species of aphelinid parasitoids (Krombein et al. 1979; Burden and Hart 1989, 1993), but the scale is also probably attacked by more generalist predators of armored scale insects, including harvestmen, crickets, earwigs, and neuropteran larvae (Clausen 1940, 1978; Crumb et al. 1941; Cloudsley-Thompson 1958; Ebling 1978; Hanks and Denno 1993). In this study, we examined the inuence of plant community structure within urban landscapes on rates of predation and parasitism of pine needle scale, scale population density, and the abundance and species diversity of the arthropod community as a whole. In another portion of this study, we excluded predators from the study trees to better evaluate the impact of parasitoids on scale populations. Finally, we tested the ability of natural enemies to disperse short distances, which is of interest because of the small spatial scale of ornamental landscapes where the scale is a pest.
2000 Entomological Society of America

0046-225X/00/13051311$02.00/0

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Chionaspis pinifoliae has long been confused with Chionaspis heterophyllae Cooley, the pine scale, because of similar appearance and natural history (Shour 1986, Kosztarab 1996). Both species overwinter in the egg stage (Kosztarab 1996) and crawlers of both species emerge synchronously in spring and summer. The two species also share parasitoid species (Burden and Hart 1993). Differences in phenology and morphology are too subtle to distinguish C. pinifoliae from C. heterophyllae in the eld (Shour 1986). The two species also overlap in geographic distribution, C. pinifoliae occurring over most of North America while C. heterophyllae is conned to the eastern and midwestern states (Shour and Schuder 1987, Kosztarab 1996). For the purposes of this report, we acknowledge the presence of the two scale species in the area of our study, but refer to the species complex as pine needle scale (see Johnson and Lyon 1988). Inuence of Plant Community Structure on Population Density of Pine Needle Scale. We estimated population densities on pine trees in three types of urban habitats: (1) impoverished habitats, ornamental landscape plantings with pines in proximity to paved roads or parking lots, and surrounded by gravel or mulch (n 25 sites); (2) turf habitats, ornamental landscapes with pines surrounded by turf (n 24 sites); and (3) wooded habitats, park-like and wooded primarily with pine species (n 24 sites). Study sites were in Champaign-Urbana, IL, and at each site there were at least three of the common hosts of pine needle scale (Shour and Schuder 1987): Pinus mugo Turra (0.252 m tall), Pinus sylvestris L. (1.5 4 m), or Pinus nigra Arnold (2.55 m). There are apparently no standard protocols for estimating population densities of scale insects on conifers (see Kozar 1990, Jactel et al. 1996). Our initial attempts to estimate density of pine needle scale by random sampling proved inaccurate at low densities because of the patchy distribution of scales within trees. Instead, we estimated population densities by examining needles distributed throughout the canopy and counting female scales for a standard 3-min period. We counted only scales of the current generation, as evidenced by an intact and pure white cover. This method was reproducible in quantifying density even of very lightly infested trees. Similar visual techniques have been used to estimate population densities of a variety of arthropod species (e.g., Wilson and Simberloff 1969, McCullough and Sadof 1998, Sebolt and Landis 1999). We estimated population densities of pine needle scale in June 1997 during the rst generation. Infesting Potted Pines with Scale. We infested small pine trees with pine needle scale to evaluate the impact of natural enemies on scale populations. Our potted pines were 25 40 cm tall Scotch pines (P. sylvestris variety French Blue) in plastic pots (1519 cm diameter) with a sterilized potting mixture of equal proportions of soil, peat, and perlite. Pines were potted in mid-April 1997 and held in a greenhouse under

long-day photoperiod, were watered as needed, and fertilized at 2-wk intervals (15:30:15; Scotts MiracleGro Products, Port Washington, NY). We infested trees with pine needle scale 1 mo after potting by laying scale-infested cuttings on them during crawler emergence; cuttings were taken from infested Scotch pine tree (Hoot Owl Christmas Tree Farm, Urbana, IL). After crawlers had settled, we disposed of cuttings to prevent parasitoids from emerging in the greenhouse. Inuence of Plant Community Structure on Rates of Predation and Parasitism. To identify the parasitoid species that attacked pine needle scale in our study area, we collected scale-infested cuttings and reared parasitoids in lidded cardboard buckets (17 cm diameter, 18 cm high) to which was attached a glass vial trap (15 mm o.d.). Parasitoids were stored in 70% ethanol and 10 specimens of each of three morphospecies were submitted for identication to the USDA Systematic Entomology Laboratory in Beltsville, MD. A fourth species, discovered later, was identied by J. M. Heraty at the University of California, Riverside. We caged predaceous arthropods with scale-infested needles of Scotch pine to conrm that they would eat pine needle scale: only species that were most likely to be predators were tested, including harvestmen (Opiliones), snowy tree crickets (Oecanthus fultoni Walker), eld crickets (Gryllus sp.), larval green lacewings (Chrysopidae), and twicestabbed lady beetles [Chilocorus stigma (Say); see Clausen 1940, 1978; Crumb et al. 1941; Cloudsley-Thompson 1958; Ebling 1978; Hanks and Denno 1993]. Predators were caged individually (n 3 per species) in plastic containers with moistened cotton rolls (to provide water) and pine needles having similar densities of female scales ( 10 scales) in the second or third instar. After 24 h, we inspected scales for evidence of predation, such as damage to scale cover or removal of the scale body. To determine whether rates of predation and parasitism were inuenced by habitat, we positioned potted Scotch pines infested with scale next to or at the base of study trees in impoverished turf and wooded habitats (n 10, 10, 15, respectively) on 16 25 June 1997. Scales on both potted and resident trees were either second or third instars, the life stages vulnerable to parasitization (unpublished data). Potted pines were subsequently watered as needed. After 5 wk, we returned the potted trees to the laboratory where they were held for 2 wk to allow parasitoids to develop. To estimate the density of scales per unit of needle length, we arbitrarily selected 20 needles from each seedling, counted the number of adult female scales on each needle, and measured needle length. To estimate percent parasitism and predation, we arbitrarily selected 50 adult female scales per tree and examined them under a dissecting microscope. In many cases the scale insects themselves were missing, but the condition of their wax covers provided evidence of activity by any natural enemies (characterized in part during studies of predation, described above). A circular exit hole was

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evidence of parasitism; predators with chewing mouthparts tore ragged holes in the cover, whereas those with sucking mouthparts left only the shriveled bodies of their prey. We excluded adult females that had been killed by fungi, as well as those from the previous generation, which were identied by having either discolored tests or discarded chorions under their tests. Impact of Parasitoids on Scale Populations Exclusive of Predators. Predators of pine needle scale apparently consumed parasitized scales and even parasitoid pupae, and therefore could inuence the role of parasitism in regulation of scale population density. To examine the impact of parasitoids in scale population density, we excluded predators from potted pines in wooded habitats where potential natural enemies of the scale were most abundant (see below), and measured parasitism rate. To exclude predators, we placed a cylinder of aluminum window screen (1 mm mesh, 60 cm tall) around scale-infested potted trees, closed at the top with staples and secured to the pot with duct tape. Preliminary experiments demonstrated that window screen excluded most, if not all, predators while permitting parasitoids access to scales. Female scales on potted trees were in the second or third instar. We positioned these potted pines next to nine Scotch pines in each of three wooded areas. After 5 wk, potted pines were returned to the laboratory to estimate percent parasitism (as described above). Evaluation of Small-Scale Movement of Natural Enemies. To evaluate dispersal abilities of natural enemies over small spatial distances, we positioned three scale-infested potted pines (female scales in second or third instar) in each of three impoverished sites so as to contact the canopy of resident trees. In the same sites, we also positioned three scale-infested pines 30 cm from the canopy edge (bare ground or gravel separated potted pines from resident trees). The study was set up on 13 August 1997 and potted pines were subsequently watered as needed. After 5 wk, pines were returned to the laboratory and held for 2 wk to allow parasitoids to develop, and then scales were examined to estimate rates of predation and parasitism (as described above). Inuence of Plant Community Structure on Abundance and Diversity of Arthropods. To examine the inuence of habitat on arthropod communities associated with host plants of pine needle scale, we took beating samples of all 73 study trees on 19 June and 27 August 1997. Samples were taken at mid-canopy from four branches per tree, one at each cardinal point. Each branch was beaten four times with a 925-g rubber mallet and falling arthropods were captured in an enamel pan partly lled with 70% ethanol. Branch samples from each tree were combined into a single sample. We categorized all collected arthropods into morphospecies and counted the specimens of each. We further categorized these morphospecies into guilds: phytophagous insects, predators, parasitoids, and potential predators of pine needle scale (our method of sampling was not effective in capturing aphelinid

parasitoids). We estimated species diversity of arthropods with the Shannon-Wiener index (H ; Peet 1974, Hayek and Buzas 1997). Statistics. We used analysis of variance (ANOVA; SAS Institute 1988) to test the effect of habitat on density of pine needle scale per tree, percent parasitism, percent predation, arthropod density, and the effect of proximity to resident pines on percent parasitism and predation. We determined whether the data met the assumptions of ANOVA by conrming homogeneity of variances between treatments (Fmaxtest) and normality within treatments (ShapiroWilks test; Sokal and Rohlf 1995). Data not suitable for ANOVA were analyzed by the nonparametric Kruskal-Wallis test (Sokal and Rohlf 1995). Differences between individual means were tested by the least signicant difference (LSD) test (Ott 1993). We compared ShannonWiener indices with the Student t-test (Magurran 1988). Data are presented as means 1 SE unless stated otherwise. Results Inuence of Plant Community Structure on Population Density of Pine Needle Scale. Density of pine needle scale varied signicantly across habitats and was highest in impoverished habitats (mean of 60 scales/tree/3-min search), intermediate in turf habitats (17 scales), and lowest in wooded habitats (two scales; ANOVA F 11.7; df 2, 62; P 0.0001). Each mean was signicantly different from the others (LSD test P 0.05). Inuence of Plant Community Structure on Rates of Predation and Parasitism. Of four parasitoid morphospecies reared from scale-infested clippings, three were aphelinids: Aphytis sp. poss. chilensis Howard, Encarsia aurantii Howard, and Coccobius varicornis (Howard). The fourth parasitoid species was in the genus Zagrammosoma (Hymenoptera: Eulophidae), most species of which are believed to be parasitoids of leafminers (Schauff et al. 1997). The relatively large body size of the Zagrammosoma sp. ( 23 mm long) also suggests it is probably not a parasitoid of pine needle scale and that it emerged from other hosts on our pine clippings. Snowy tree crickets, eld crickets, and green lacewing larvae all readily fed on female pine needle scales in cages. Twicestabbed ladybird beetles and harvestmen did not eat scales on individual needles, but did so on scale-infested Scotch pine trees in an independent laboratory experiment. Thus, we considered all of these species potential predators of pine needle scale. On scale-infested potted pines placed in the eld, parasitism rate was highest in impoverished habitats (where the scale was most abundant), intermediate in turf habitats, and very low in wooded habitats (where the scale was rare; means signicantly different; KruskalWallis statistic 16.7, df 2, P 0.0002; Table 1). Parasitism rates across all three habitats were signicantly and positively correlated with host abundance on resident trees (Fig. 1), at least at the spatial

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Table 1. Parasitism rates and predation rates of pine needle scale (mean SE) on Scotch pine seedlings placed in three habitats n Impoverished Turf Wooded
a b

Parasitism rate, % 26 17 1 7.7a 3.9b 0.4c

Predation rate 1,a (%) 42 41 37 9.0a 8.6a 5.8a

Predation rate 2,b (%) 59 52 54 9.4a 9.5a 6.4a

25 24 24

Only scales with obvious evidence of predation. As in predation rate 1, but including scales that died before oviposition and were assumed to have been killed by predators.

scale of individual potted trees. This suggests that parasitoids were more abundant in areas where densities of pine needle scale were high. Parasitism rate was not correlated with scale density of individual potted pines (regression analysis, t 0.42; P 0.67). Predation rates of pine needle appeared to be highest in impoverished habitats, but differences between habitats were not statistically signicant (ANOVA, F 0.107; df 2, 61; P 0.89; Table 1). Impact of Parasitoids on Scale Populations Exclusive of Predators. Even when predators were excluded by caging pine trees with aluminum screen, parasitism rates of scales in wooded habitats were very low (0.0034 0.003; n 9), suggesting that parasitoids were scarce in that habitat. Evaluation of Small-Scale Movement of Natural Enemies. Neither parasitism nor predation rates of pine needle scale differed signicantly between potted pines positioned in contact with foliage of resident trees (parasitism rate 0.71 0.08, predation rate 0.11 0.03) and those positioned 30 cm away (parasitism rate 0.62 0.10, predation rate 0.11 0.04; KruskalWallis statistics 0.56 and 0.002, df 1, P 0.45 and 0.96, respectively). These ndings conrmed that natural enemies would disperse short distances in search of scale prey. Inuence of Plant Community Structure on Abundance and Diversity of Arthropods. Our beating samples of 73 trees yielded 2,887 arthropod specimens of

Fig. 1. Relationship between mean parasitism rate of pine needle scale on potted trees placed in three habitats and the number of scales on resident pine hosts counted in a 3-min search. Best t regression equation: Y 0.13X 6.06, n 22, r2 0.45; P 0.0006.

75 morphospecies. The number of specimens of each species ranged from 1 to 376 individuals, averaging 27.4 67.1 specimens per species (mean SD). The frequency distribution of the number of specimens per morphospecies was skewed strongly to the right (skewness, 3.81): 18 morphospecies were represented by only one specimen, nine by two specimens, and eight by three specimens. The remaining 40 morphospecies were represented by ve or more individuals. The abundance of all arthropods (the mean number of individuals collected per sample) was highest in impoverished habitats (44.1 7.9 individuals per sample), intermediate in turf habitats (29.1 7.2 individuals), and lowest in wooded habitats (19.8 2.2 individuals) (F 4.39; df 2, 62; P 0.02; individual means signicantly different, LSD test P 0.05). Species diversity of arthropods in impoverished habitats (H 2.51), however, was 5% lower than in turf habitats (H 2.65; t-test P 0.0005) and 20% lower than in wooded habitats (H 3.13; t-test P 0.0005). Diversity did not differ signicantly between impoverished and turf habitats (t-test P 0.05). Phytophagous species (primarily aphids, leafhoppers, and thrips) were more abundant in impoverished habitats (19.1 3.6 individuals) than in turf (17.4 4.7) and wooded habitats (8.95 1.9), although variability in abundance within habitats resulted in a lack of statistical signicance (F 2.93; df 2, 61; P 0.061). Species diversity of phytophagous species was lower in impoverished (H 1.37) and turf habitats (H 1.35) than in wooded habitats (H 1.68), but these differences were also not signicant (t-test P 0.05). Abundance of predaceous arthropods (primarily harvestmen, ladybird beetles, lacewings, and spiders) also did not vary signicantly with habitat (2.0 0.3 individuals in impoverished habitats, 2.7 1.3 in turf habitats, 2.8 0.8 in wooded habitats; F 0.32; df 2, 61; P 0.05), nor did species diversity of predators (impoverished H 1.33, turf H 1.41, wooded H 1.54; t-tests P 0.05). Parasitoids (primarily braconids, encyrtids, eupelmids, and mymarids) as a group were nearly equally abundant in all habitats (0.7 0.2 in impoverished habitats, 0.5 0.2 in turf habitats, 0.6 0.2 specimens in wooded habitats; F 0.24; df 2, 61; P 0.79), although they were signicantly less diverse in impoverished habitats (H 1.09) and turf habitats (H 0.97) than in wooded habitats (H 2.01; t-tests P 0.0005 and P 0.0005, respectively). Potential predators of pine needle scale (harvestmen, earwigs, crickets, neuropteran larvae, coccinellids) did not vary signicantly in abundance across habitats (1.12 0.26 individuals in impoverished habitats, 0.80 0.30 in turf habitats, 1.92 0.66 in wooded habitats; F 1.38; df 2, 61; P 0.26), but species diversity was 30% higher in impoverished than wooded habitats (impoverished H 1.30, wooded H 1.03; t-test P 0.05).

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Higher species diversity of arthropods in wooded habitats than in impoverished habitats was consistent with a positive association between arthropod diversity and plant species diversity reported for other managed and natural systems (Risch 1981, Hanks and Denno 1993, Yue et al. 1994, Dean and Milton 1995, Shrewsbury 1996). Nevertheless, arthropods (especially phytophagous species) were most abundant in impoverished habitats, suggesting that their populations were poorly regulated in those habitats, despite equal abundance of predators and parasitoids across habitats. Ours is the rst report that pine needle scale is parasitized by Encarsia aurantii, a cosmopolitan species that attacks 20 species of armored scale insects (Krombein et al. 1979). Aphytis chilensis, however, is a known parasitoid of C. pinifoliae, C. heterophyllae, and two other scale species (Krombein et al. 1979, Burden and Hart 1993) and is cosmopolitan (DeBach and Rosen 1991). Aphytis chilensis may represent a complex of sibling species (Krombein et al. 1979). Coccobius varicornis is also a known parasitoid of C. pinifoliae and C. heterophyllae and nine other species of scale insects, and is native to eastern North America (Krombein et al. 1979, Burden and Hart 1993). It is unlikely that variation in the abundance of pine needle scale across habitats was related to host plant quality: armored scales have higher survivorship on unstressed hosts (Cockeld and Potter 1986, Hanks and Denno 1993), but pine needle scale was most abundant in impoverished, unnatural habitats where trees were likely subjected to environmental stress (e.g., Krizek and Dubik 1987, Clark and Kjelgren 1989, Cregg 1995). This apparent paradox may be explained in part by the lack of effective natural enemies of pine needle scale in impoverished areas; scale populations reached high densities even though host quality was suboptimal. Higher parasitism rates of pine needle scale in impoverished habitats, where the scale was most abundant, suggest that aphelinids do not effectively regulate scale populations in urban habitats as has been observed in another armored scale species (Hanks and Denno 1993). The small size and short life span of aphelinids presumably limit their ability to y long distances in search of hosts (Viggiani 1984); they may prefer to remain in proximity to pines infested with the scale, rather than dispersing. Nevertheless, the wasps readily traveled the 30 cm from infested trees to parasitize scales on potted trees, demonstrating that they do disperse short distances. Dispersal also explains higher rates of parasitism on potted trees positioned near resident trees that supported high-density scale populations (Fig 1). Rates of parasitism in wooded habitats were low, suggesting that parasitoids were scarce in these habitats. Though there is a possibility that our excluders hindered parasitoids, parasitism rates were also low in the same habitat when scales were on potted trees without screen.

Rates of predation also were similar across habitats. However, we may have underestimated the impact of predators on pine needle scale populations because scales on our potted pine trees were available to predators for only a short time, whereas those on resident pines were exposed their entire lives, providing the predator guild a greater opportunity to respond to changes in scale density. Moreover, we did not assess predation rate in the rst instar, and this source of mortality may greatly inuence population dynamics of scale insects (Yang and Sadof 1995, Eliason and McCullough 1997). We also may not have detected differences between habitats in the abundances of predators because of limitations in our sampling methods; we sampled arthropods only from host plants of pine needle scale and so did not evaluate abundance of important generalist predators on other plant species. For example, plant species other than the host plant are the source of highly mobile predators of azalea lacebug, Stephanitis pyrioides (Scott) (P. Shrewsbury, personal communication). The rarity of pine needle scale in wooded habitats suggests that this pest might be managed in ornamental landscapes by manipulating plant species diversity and structural complexity to foster natural enemies. For example, the parasitoid A. chilensis feeds on pollen of white clover (Trifolium repens L.) and is attracted to its oral volatiles (Tooker 1999); planting white clover, or other plant species that provide oral resources, in plantations of Christmas trees or in ornamental landscapes may encourage A. chilensis to suppress scale populations. Augmentation of plant diversity in these habitats also will favor predators by providing a greater diversity and abundance of alternative prey and suitable microhabitats.

Acknowledgments
We thank May Berenbaum, Robert Wiedenmann, Cliff Sadof, Paula Shrewsbury, Eileen Eliason, and an anonymous reviewer. We are grateful for help and research assistance provided by Charlie Helm, Art Zangerl, and Megan Weaver. Thanks also to Hensler Nurseries for donating pine seedlings and to Dave Clark of Hoot Owl Tree Farm, Charles Wilson of Wilson Tree Farm, and the management of Marketplace Mall and Good Vibes for use of their property. We thank Michael Schauff (USDA Systematic Entomology Laboratory) and John Heraty (University of California, Riverside) for identifying parasitoid species. This work was in partial fulllment of a M.S. degree for J.F.T. from the University of Illinois at Urbana-Champaign and was supported in part by USDA NRI Grant No. 99-35316 7850 to L.M.H.

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