COMMUNITY AND ECOSYSTEM ECOLOGY Attractiveness of Michigan Native Plants to Arthropod Natural Enemies and Herbivores A. K. FIEDLER1 AND D. A. LANDIS Department of Entomology, 204 Center for Integrated Plant Systems, Michigan State University, East Lansing, MI 48824-1311 KEY WORDS native plant, habitat management, natural enemy, conservation biological control Conservation biological control involves practices that protect and enhance natural enemies already present in the landscape by decreasing natural enemy mortality or providing resources that enhance natural enemy survival and efÞcacy (Ehler 1998). Using plants to provide needed resources to natural enemies, termed habitat management, is a growing focus of conservation biological control (Landis et al. 2000). Habitat management can provide natural enemies with alternate hosts (DeBach and Rosen 1991, Menalled et al. 1999, van Emden 2003), shelter (Gurr et al. 1998), and nonhost food (Baggen et al. 1999, Wilkinson and Landis 2005) in ways that enhance biological control (Gurr et al. 2003, Wratten et al. 2003). Both parasitoids and predators beneÞt from access to nonhost food, especially nectar and pollen. For parasitoids, access to nectar may be crucial for adult survival in species that do not host feed (Jervis and Kidd 1986). Several laboratory studies have shown increased longevity and/or fecundity of adult parasitoids with access to nectar or sugars (Dyer and Landis 1996, Baggen et al. 1999, Wäckers 1999). At points in 1 Corresponding author, e-mail: Þedlera@msu.edu. some parasitoid life cycles, access to sugars may be more important than host availability (Baggen and Gurr 1998). Although predators frequently use prey resources as adults, they often supplement their diets with plant resources including phloem ßuids (Eubanks and Denno 1999) and pollen (Harmon et al. 2000). In some cases, predators may require protein garnered from ßower pollen to mature eggs or access to pollen may increase fecundity (Hickman and Wratten 1996). To maximize the beneÞt of habitat management, plant species must be carefully selected. Many natural enemies cannot access nectar in ßowers with deep, narrow corollas, because their mouthparts are not specialized for ßower-feeding (Jervis et al. 1993, Orr and Pleasants 1996, Wäckers et al. 1996). In addition, plant and insect phenology must coincide so that insects garner beneÞts of access to nectar and pollen at the correct time to increase their populations (Jervis et al. 1993, Orr and Pleasants 1996, Colley and Luna 2000, Siekmann et al. 2001). Finally, screening plants to select those which provide resources to natural enemies and not herbivorous pests is an important consideration (Baggen and Gurr 1998, Baggen et al. 0046-225X/07/0751Ð0765$04.00/0 䉷 2007 Entomological Society of America Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Environ. Entomol. 36(4): 751Ð765 (2007) ABSTRACT The use of plants to provide nectar and pollen resources to natural enemies through habitat management is a growing focus of conservation biological control. Current guidelines frequently recommend use of annual plants exotic to the management area, but native perennial plants are likely to provide similar resources and may have several advantages over exotics. We compared a set of 43 native Michigan perennial plants and 5 frequently recommended exotic annual plants for their attractiveness to natural enemies and herbivores for 2 yr. Plant species differed signiÞcantly in their attractiveness to natural enemies. In year 1, the exotic annual plants outperformed many of the newly established native perennial plants. In year 2, however, many native perennial plants attracted higher numbers of natural enemies than exotic plants. In year 2, we compared each ßowering plant against the background vegetation (grass) for their attractiveness to natural enemies and herbivores. Screening individual plant species allowed rapid assessment of attractiveness to natural enemies. We identiÞed 24 native perennial plants that attracted high numbers of natural enemies with promise for habitat management. Among the most attractive are Eupatorium perfoliatum L., Monarda punctata L., Silphium perfoliatum L., Potentilla fruticosa auct. non L., Coreopsis lanceolata L., Spiraea alba Duroi, Agastache nepetoides (L.) Kuntze, Anemone canadensis L., and Angelica atropurpurea L. Subsets of these plants can now be tested to develop a community of native plant species that attracts diverse natural enemy taxa and provides nectar and pollen throughout the growing season. 752 ENVIRONMENTAL ENTOMOLOGY 5 of the most widely recommended annual resource plants that are exotic in Michigan. The goal of this process was to select a subset of plants for further consideration in a habitat management program. Our hypotheses were that (1) plant species would vary in attractiveness to natural enemy arthropods, (2) some native plants would be as or more attractive to natural enemy arthropods as frequently recommended exotics, (3) plant species would attract different numbers and types of natural enemy and herbivore taxa, and (4) attractiveness would increase as perennial plants matured. Materials and Methods Plant Selection Criteria. We selected 43 species of Michigan native plants for study using the following criteria: (1) native Michigan perennials, (2) adapted to nonirrigated agricultural Þeld conditions (full sun, moderate drought periods likely), (3) represent a diversity of bloom periods from early through late season, (4) from a variety of plant families, (5) varied ßoral color and morphology, (6) forb or shrub species formerly common in Michigan prairie and oak savanna habitats, and (7) commercially available Michigan genotypes. Native plants were selected in consultation with a Michigan native plant nursery owner (W. D. Schneider, personal communication). Five plant species exotic to Michigan were also selected for study based on the following criteria: (1) commonly recommended to enhance beneÞcial insects and (2) Þt criteria 2Ð 4 above. All of the frequently used nonnatives were annuals, reßecting the prevalence of annuals in habitat management studies. Study Site. An agricultural Þeld on the Michigan State University Entomology Farm in Ingham County, MI, was selected for this study. Soil type consisted of a Marlette Þne sandy loam, and the Þeld was most recently farmed in a corn-soybean rotation. Plants were established in 1-m2 blocks spaced 6 m apart within a matrix of orchardgrass (Dactylis glomerata L.), a species commonly found in the surrounding landscape, that was regularly mowed to prevent ßowering. The experiment was conducted in a randomized complete block design with Þve replicates of each of the 43 native Michigan perennial plants and the 5 exotic plant species. Native plants were obtained as rooted plugs (Wildtype Design Native Plants & Seeds, Mason, MI) and planted in September 2003. Plant densities of three, Þve, or eight plants per plot were selected based on individual species characteristics such that the plot would be densely Þlled with plant material at maturity (Fiedler 2006). Exotic annual species were planted for comparison to native species, as follows. Vicia faba (cultivar Windsor; JohnnyÕs Seeds, Winslow, ME) was seeded on 20 May 2004 and on 9 May 2005. Sixteen plugs/m2 of L. maritima (cultivar Snow Crystals Ball Seed Company, Chicago, IL) were planted on 20 May 2004 and 16 June 2005. On 29 May 2004 and 9 May 2005, A. graveolens (cultivar Mammoth island, C. sativum Spice Coriander) (Richters Herb Specialists, Goodwood, Ontario, Canada), Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 1999, Lee and Heimpel 2005, Winkler 2005, Ambrosino et al. 2006, Begum et al. 2006, Lavandero et al. 2006). When the goal of a habitat management program is to increase plant resource availability to beneÞcial insects, several methods have been used to test which plants are most attractive to natural enemies. The most controlled are laboratory studies of speciÞc plantÐ insect interactions that consider whether speciÞc natural enemies can access and feed on plant nectar or pollen of speciÞc ßowering plants (Patt et al. 1997, Baggen and Gurr 1998, Baggen et al. 1999). Another tactic is the use of observational studies of insects using plants already growing in an area to determine which are most frequently visited by natural enemies (van Emden 1963, Bugg et al. 1987, Jervis et al. 1993, Bugg and Waddington 1994, Idris and GraÞus 1995, Tooker and Hanks 2000). A third is to select a group of plants based on previous success and establish them individually (White et al. 1995, Hickman and Wratten 1996) or in plant groupings (Chaney 1998, Nentwig et al. 1998, Nicholls et al. 2001, Frank and Shrewsbury 2004, Rebek et al. 2005, Pontin et al. 2006) and assess the number and type of natural enemies in the planting or nearby Þeld. None of these studies, however, have established replicated groups of plant species and compared their individual attractiveness to natural enemies. Nonindigenous plants have often been the focus of habitat management. In part, this is because a small group of effective plants have been repeatedly used worldwide. These include alyssum (Lobularia maritima L. Desv.), borage (Borago officinalis L.), and coriander (Coriandrum sativum L.), native to the Mediterranean and Southern Europe, dill (Anethum graveolens L.) and buckwheat (Fagopyrum esculentum Moench), native to Asia, faba bean (Vicia faba L.), native origin unknown, possibly the Mediterranean, and phacelia (Phacelia tanacetifolia Benth), native to California. Many of these plants are also annual, which provides planting and ßowering ßexibility but precludes potential beneÞts of establishing more permanent habitats. Although most guidelines recommend annual plants not native to the management area (Dufour 2000), there is no reason to suspect that perennial native plants cannot perform as well as annual exotics. Use of native perennial plants for habitat management has several beneÞts. These species are adapted to the local environment. They add to native biodiversity and may be used to restore imperiled habitats. Finally, they are less likely to be invasive than exotic annuals. In addition, their perennial habit provides natural enemy overwintering sites and results in a one-time seed or plant purchase and establishment of plants compared with yearly establishment of annual species. Despite the extensive literature on habitat management, there is a lack of studies using a screening process that examines the entire natural enemy and herbivore community visiting single plant species with adequate replication. Our objective was to compare the attractiveness to natural enemy and herbivore arthropods of 43 Michigan native perennial plants and Vol. 36, no. 4 August 2007 FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS plant in 2004 and 2005 (PROC REG; SAS Institute 2003). A two-way analysis of variance (ANOVA) with block and plant species as factors was conducted on the mean insect counts for the 3-wk full bloom period (PROC GLM; SAS Institute 2003). Plant species were divided into three categories for ANOVA analyses according to timing of peak bloom: early season (May to June), midseason (July to 20 August 2004 and July to 9 August 2005), or late season (21 August 2004 and 10 August 2005 to October). Because of lack of homogeneity of variance between treatments, data for early season 2004 and mid- and late season 2005 were analyzed using a weighted least squares approach based on a separate variance estimate for each treatment, which yields fractional denominator degrees of freedom (Kutner et al. 2005). Least squares means separations were performed with a Tukey adjustment and SatterthwaiteÕs adjustment for degrees of freedom (␣ ⫽ 0.05) (Satterthwaite 1946). Results A total of 41 and 48 of the tested plant species bloomed in 2004 and 2005, respectively. Individual species bloomed from early May through September in 2004 and May through 4 October in 2005 and had similar bloom periods from year to year except where noted (Table 1). In both years, natural enemy numbers at most plants increased signiÞcantly throughout the season (2004: week F ⫽ 33.49, P ⬍ 0.001, R2 ⫽ 0.46; 2005: week F ⫽ 19.96, P ⬍ 0.001, R2 ⫽ 0.30) (Fiedler and Landis 2007). In 2004, the most attractive plant in the early season averaged 11.6 natural enemies per sample during full bloom period, whereas mid- and late season plants averaged 33.0 and 86.4 natural enemies per sample, respectively. During full bloom period in 2005, the most attractive plants had 31.9, 33.1, and 199.9 insects per sample in the early, mid-, and late seasons, respectively. Overall natural enemy numbers were lower in 2004 than in 2005, with season-long averages of 13.8 and 20.5 per plant species per sample, respectively. In both 2004 and 2005, there was a signiÞcant species effect on the mean number of natural enemies collected during full bloom period, indicating that species differed signiÞcantly in their attractiveness to natural enemies (2004: early season, F ⫽ 23.16, df ⫽ 7.88, P ⬍ 0.001; midseason, F ⫽ 29.26, df ⫽ 48, P ⬍ 0.001; late season, F ⫽ 8.78, df ⫽ 58, P ⬍ 0.001; 2005: early season, F ⫽ 23.59, df ⫽ 51, P ⬍ 0.001, midseason, F ⫽ 53.67, df ⫽ 6.84, P ⬍ 0.001, late season, F ⫽ 32.27, df ⫽ 6.13, P ⫽ ⬍0.001). Within the native plants alone, signiÞcant effects on natural enemy attractiveness were also found in both years (2004: early season, F ⫽ 15.86, df ⫽ 8.25, P ⬍ 0.001; midseason, F ⫽ 9.74, df ⫽ 36, P ⬍ 0. 001; late season, F ⫽ 7.72, df ⫽ 50, P ⬍ 0.001; 2005: early season, F ⫽ 24.53, df ⫽ 47, P ⬍ 0.001; midseason, F ⫽ 43.63, df ⫽ 7, P ⬍ 0.001; late season, F ⫽ 33.59, df ⫽ 5.87, P ⬍ 0.001), indicating that native plants varied signiÞcantly in their attractiveness. There was no signiÞcant effect of block (P ⬍ 0.05) except in late season 2005, when plants in block four attracted signiÞcantly fewer insects (F ⫽ 3.18, df ⫽ 4, P ⫽ 0.020). Block 4 was Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 and F. esculentum (cultivar Mancan; Simmons Family Farms, North Branch, MI) were seeded. To maintain background fertility for the orchardgrass, granular nitrogen (urea or ammonium nitrate, 33.6 kg N/ha) was applied to the entire Þeld on 23 June 2004 and 14 April 2005. In response to apparent nutrient deÞciencies in particular plant species, we applied liquid fertilizer (5.7 liters of 20 Ð20-20; Peters professional all-purpose plant food, Spectrum Group, St. Louis, MO) on 23 June 2004 to Ceanothus americanus L., Monarda punctata L., Sambucus racemosa L., Hydrophyllum virginianum L., Amorpha canescens (Pursh), and Aquilegia canadensis L. Flower Phenology. We observed all plants weekly for occurrence of open ßowers with dates of Þrst, last, and peak bloom recorded for each species. Hereafter, we use “peak bloom” to refer to the speciÞc week of maximum ßoral display for each species and “full bloom period” to the week of peak bloom and 1 wk on either side. Arthropod Collection. From May through September 2004 and 2005, we sampled arthropods weekly from ßowering plants between the hours of 0930 Ð1330 EST on sunny days with winds ⬍5 mph. For analysis, we used samples from the full bloom period to reduce the inßuence of week-to-week variability in insect catch caused by weather and plant phenology. To collect insects, a Þne mesh white no-see-um netting bag (Kaplan Simon Co., Braintree, MA) was placed over the intake on a gas-powered leaf vacuum (Stihl BG55, Norfolk, VA). Each plot was vacuumed until all ßowers were sampled (limited to 30 s in 2004) (Rebek et al. 2005). To compare the number of insects on ßowering plants versus background plants, we placed a 1-m2 PVC quadrat in the mown orchardgrass matrix in each of Þve blocks and vacuum sampled the quadrat weekly from 21 June through September 2005. These samples are subsequently referred to as “grass control.” Insects were frozen, identiÞed to family, separated into natural enemies, herbivores, and “other,” and counted. Insects from any predaceous or parasitic family, or genus or species within a family known to be predaceous or parasitic, were included as natural enemies. Insects from any family known to be broadly herbivorous were counted as herbivorous insects. Attractiveness here is based on the number of arthropods collected per sample, and as such, it is a measurement of attraction to, arrestment at, and tenure time on the plant species. Taxonomy. Insect taxonomic classiÞcation follows Triplehorn and Johnson (2005), and plant nomenclature follows Voss (1996). Insect vouchers were deposited in the Michigan State University Entomology Museum, and plant vouchers were deposited in the Michigan State University Herbarium. Statistical Analysis. Numbers of natural enemies per ßowering plant and block were log10(x ⫹ 1)-transformed to better Þt assumptions of normality and homogeneity of variance. A simple regression was conducted between the log10 (x ⫹ 1) number of natural enemies and the week of peak bloom for each 753 754 Table 1. ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 4 Flowering phenology 2005 Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Plants are listed in order of bloom. Exotic plant names are underlined. f, peak bloom date; 䡲, full bloom; Ñ, in bloom. a Observed 2004 peak bloom dates were Aug. 31 for C. lanceolata and P. fruticosa, and Aug. 13 for A. nepetoides. b Did not bloom in 2004. on a slight elevation, and plants there may have experienced more moisture stress during the particularly dry 2005 growing season. Early Season. In 2004, the native Heracleum maximum (Bartr.) was signiÞcantly more attractive than other plants (Fig. 1a). Exotic L. maritima and natives August 2007 FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS 755 Fragaria virginiana Duchesne were the next most attractive group. In 2005, Angelica atropurpurea L., which did not bloom in 2004, and Coreopsis lanceolata L. were the most attractive plants to natural enemies. Anemone canadensis, Zizia aurea L. Koch, Penstemon hirsutus L. Willd., H. maximum, and F. virginiana were the next most attractive plants but overlapped in signiÞcance with the least attractive species (Fig. 1b). Samples taken from 21 June 2005 onward show that A. atropurpurea, C. lanceolata, A. canadensis, P. hirsutus, and H. maximum attracted more natural enemies than a neutral grass background (grass control) during the same period. Although no grass samples were taken when Z. aurea and F. virginiana were blooming, these species attracted more natural enemies than other plants blooming in May and early June. In both 2004 and 2005, no natural enemies were collected at Aquilegia canadensis L., even though abundant blossoms were present. L. maritima and H. maximum were relatively less attractive in 2005 than in 2004. Overall, Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 1. Early season mean number of natural enemies collected per 1-m2 plot the week during the full bloom period for each species (peak bloom dates 1 May to 21 June) (a) 2004 and (b) 2005. Plants listed in 2005 bloom order from left to right. 2004 samples were limited to 30 s; in 2005, plots were sampled until all ßowers were sampled. Grass controls were sampled from 21 June 2005 onward only. For A. canadensis, P. hirsutus, and A. atropurpurea, the corresponding grass control points represent the mean of one date; remaining points represent the mean of two dates. Although not in full bloom at this time, L. maritima is included as the only exotic comparison plant blooming in early season. Bars with different letters within a Þgure are signiÞcantly different using Tukey-adjusted means comparisons (P ⬍ 0.05). 756 ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 4 however, plants attracted more natural enemies in 2005 than in 2004 during the early season, with several plants averaging 4 Ð 60 times more natural enemies in 2005 than in 2004, e.g., Z. aurea, Anemone canadensis, P. hirsutus, H. virginiana, and F. virginiana. Midseason. In 2004, the exotics F. esculentum, C. sativum, and V. faba were far more attractive than any of the native plants (Fig. 2a). However, in 2005, Apocynum cannabinum L., Potentilla fruticosa auct. non L., Spiraea alba Duroi, the exotic V. faba, Ratibida pinnata (Vent.) Barnh., exotic F. esculentum, Oenothera biennis L., and Verbena stricta Vent. were the most attractive plants (Fig. 2b). The remaining plant species were not signiÞcantly more attractive than the least attractive species and did not attract more natural enemies than grass controls from the same period. All midseason native plants attracted more natural enemies in 2005 than in 2004, including P. fruticosa. Overall, many of the plants were far more attractive in 2005 than in 2004, except the annual exotics F. esculentum and C. sativum, which had fewer natural enemies in 2005 than in 2004. Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 2. Midseason mean number of natural enemies collected per 1-m2 plot during the full bloom period for each species in (a) 2004 and (b) 2005 (peak bloom dates 1 July to 20 August 2004 and 1 July to 9 August 2005). Plants listed in 2005 bloom order from left to right. 2004 samples were limited to 30 s; in 2005, plots were sampled until all ßowers were sampled. Grass controls are a mean from the 3-wk full bloom period for each ßowering species. Bars with different letters within a Þgure are signiÞcantly different using Tukey-adjusted means comparisons (P ⬍ 0.05). August 2007 FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS 757 Late Season. In 2004, several native species attracted as many or more natural enemies as one or more of the exotics (Fig. 3a). E. perfoliatum L. and L. maritima attracted signiÞcantly more insects than many other species. Aster novae-angliae L., Solidago riddellii Frank ex Riddell, Aster laevis L., Anethum graveolens L., Lobelia siphilitica L., and Helianthus strumosus L. formed the next most attractive group but overlapped broadly with the least attractive plants. In 2005, the exotic A. graveolens was decimated by Papilionidae larvae and therefore was less attractive than many other species (Fig. 3b). Native E. perfoliatum was signiÞcantly more attractive than any other plant species, and Monarda punctata L., exotic L. maritima, natives Silphium perfoliatum L., S. riddellii, Vernonia missurica Raf., Solidago speciosa Nutt., A. novae-angliae, and H. strumosus all attracted ⬎25 natural enemies on average. All but three plant species were more attractive to natural enemies than the grass control, whereas species listed above attracted more than twice as many natural enemies as the grass control. Overall, native plants blooming before September performed better in 2005 than in 2004, including E. perfoliatum, M. punctata, V. missurica, and Cacalia atriplicifolia L., which were over twice as attractive to natural enemies in 2005 as in 2004. A group of species blooming from mid-Sep- Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 3. Late season mean number of natural enemies collected per meter squared during the full bloom period for each species in (a) 2004 and (b) 2005 (peak bloom dates 21 August to 21 September 2004 and 10 August to 27 September 2005). Plants listed in 2005 bloom order from left to right. 2004 samples were limited to 30 s; in 2005, plots were sampled until all ßowers were sampled. Grass controls are a mean from the 3-wk full bloom period for each ßowering species. Bars with different letters within a Þgure are signiÞcantly different using Tukey-adjusted means comparisons (P ⬍ 0.05). Note change in y axis scale from Figs. 2 and 3. *A. graveolens underwent heavy herbivory by Papilionid larvae in 2005. 758 ENVIRONMENTAL ENTOMOLOGY Table 2. Proportion of total natural enemies collected in 2005 at all flowering plants by order and family Order Table 3. Proportion of total herbivore hexapods collected in 2005 at flowering plants by order and family Order Number Percent total 928 6.56 Anthocoridae Miridae Nabidae 4,259 918 153 30.11 6.49 1.08 Aeolothripidae 119 0.84 Thysanoptera Cantharidae Carabidae Coccinellidae 1,542 28 587 10.90 0.20 4.15 Coleoptera Chrysopidae 69 0.49 Braconidae Bethylidae Chalcidoidea Cynipoidea Ichneumonidae Sphecidae Vespidae 225 13 3,485 441 74 78 95 1.59 0.09 24.64 3.12 0.52 0.55 0.67 Bombyliidae Dolichopodidae Empididae Stratiomyidae Syrphidae Tachinidae Total: 22 75 857 20 144 12 14,144 0.16 0.53 6.06 0.14 1.02 0.08 100.00 Family Arachnida Hemiptera Vol. 36, no. 4 Family Number Percent total Aphididae Cercopidae Cicadellidae Miridae Pentatomidae Tingidae 2,856 174 1,545 8,850 163 111 14.67 0.89 7.94 45.46 0.84 0.57 867 4.45 Arctiidae Gelechiodea Noctuidae Nymphalidae Pyralidae 217 2,890 123 14 777 76 248 101 119 12 15 36 1.11 14.84 0.63 0.07 3.99 0.39 1.27 0.52 0.61 0.06 0.08 0.18 Anthomyiidae Tephritidae Total: 242 32 19,468 1.24 0.16 100.00 Hemiptera Thysanoptera Thripidae Coleoptera Neuroptera Hymenoptera Orthoptera Lepidoptera Diptera Diptera Many Arachnida were immature and unidentiÞable to family. Numbers in order rows represent specimens not identiÞed to family level. Taxa comprising less than 0.05% not included. tember on performed similarly and quite well in both years, whereas exotics A. graveolens and L. maritima had fewer natural enemies in 2005 than in 2004. Natural Enemy Taxa. The relative proportions of natural enemy taxa collected were similar in 2004 and 2005 (Fiedler 2006). Hemiptera and Hymenoptera were the most common orders collected, followed by Coleoptera (Table 2). Within order, Anthocoridae and Chalcidoidea were the most common natural enemy groups, followed by Cantharidae, Arachnida, and Miridae (Plagiognathus politus Uhler) (Table 2). The most numerous beetles were Cantharidae. Arachnida were composed of Thomisidae, Salticidae, Tetragonathidae, Aranaeidae, and Lycosidae. Many Arachnida, however, were immatures and unidentiÞable to family. The most numerous Hemiptera were Anthocoridae. Predatory Aeolothripidae composed 14% of total thrips in 2005 (Table 2). The most common Hymenoptera were Chalcidoidea, and the most numerous Diptera collected were Empididae. The most common natural enemy arthropods in grass controls were Chalcidoidea (especially Mymaridae), Nabidae, Thomisidae, Staphylinidae, and Cynipoidea. Several groups, Mymaridae, Nabidae, and Staphylinidae, were also more common in grass than in ßowering plant samples. Plant Attractiveness to Herbivores. In both 2004 and 2005, plants that were more attractive to natural enemies were also generally more attractive to herbiv- Lepidoptera is composed of larvae and unidentiÞable adults. Numbers in order rows represent specimens not identiÞed to family level. Taxa comprising less than 0.05% not included. orous insects (Figs. 4Ð 6), although exceptions occur. For example, H. maximum was attractive to natural enemies but not herbivores in 2004 (Fig. 4a), whereas the opposite was true for Heuchera americana L. Species that attracted greater numbers of natural enemies than herbivores in early season 2004 included F. virginiana, S. obovatus, H. maximum, and C. lanceolata. In 2005, only Anemone canadensis and A. atropurpurea had greater natural enemy than herbivore abundance (Fig. 4b). During midseason, the exotic plants, notably V. faba, attracted more herbivores than the background grass controls. In 2004, the native P. fruticosa was the one plant notably more attractive to natural enemies than herbivores (Fig. 5a). In 2005, the most attractive mid season native plants all were more attractive to herbivores than natural enemies (Fig. 5b). SpeciÞcally, P. fruticosa, A. cannabinum, V. stricta, R. pinnata, and O. biennis all had greater numbers of herbivores than natural enemies. In the late season, herbivores at many ßowering species were relatively less abundant than in the early and midseason. In 2004, E. perfoliatum, L. siphilitica, S. perfoliatum, and H. strumosus all were more attractive to natural enemies than herbivores, whereas the opposite was true for S. speciosa (Fig. 6a). In 2005, M. punctata, V. missurica, S. perfoliatum, C. atriplicifolia, E. perfoliatum, H. strumosus, and S. riddellii all were more attractive to natural enemies than herbivores, whereas the opposite was true for L. maritima and S. speciosa (Fig. 6b). The most common herbivores collected in grass controls differed somewhat from those at ßowering Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Cerambycidae Chrysomelidae Curculionidae Elateridae Scarabaeidae August 2007 Table 4. tolerances FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS 759 The 23 Michigan native plant species best suited to attract natural enemy insects with bloom, plant physiognomy, and moisture 2005 peak bloom date Common name Genus and species Plant type Tolerance e e e e e e e m m m m m m l l l l l l l l l l 24 May 6 June 14 June 14 June 14 June 21 June 21 June 12 July 12 July 2 Aug. 2 Aug. 9 Aug. 9 Aug. 16 Aug. 16 Aug. 23 Aug. 23 Aug. 23 Aug. 23 Aug. 30 Aug. 13 Sept. 20 Sept. 27 Sept. Wild strawberry Golden alexanders Canada anemone Penstemon Angelica Cow parsnip Sand coreopsis Shrubby cinquefoil Indian hemp Hoary vervain Yellow coneßower Evening primrose Meadowsweet Yellow giant hyssop Horsemint Ironweed Cup plant Boneset Blue lobelia Pale-leaved sunßower RiddellÕs goldenrod New England aster Smooth aster Fragaria virginiana Duchesnea Zizia aurea L. Koch Anemone canadensis L.a Penstemon hirsutus L. Willd. Angelica atropurpurea L.a Heracleum max Bartr.a Coreopsis lanceolata L. Potentilla fruticosa auct. non L. Apocynum cannabinum L.b Verbena stricta Vent. Ratibida pinnata (Vent.) Barnh. Oenothera biennis L.c Spiraea alba Duroi Agastache nepetoides (L.) Kuntze Monarda punctata L. Vernonia missurica Raf. Silphium perfoliatum L. Eupatorium perfoliatum L. Lobelia siphilitica L. Helianthus strumosus L. Solidago riddellii Frank ex Riddelld Aster novae-angliae L. Aster laevis L. Forb Forb Forb Forb Forb Forb Forb Shrub Forb Forb Forb Forb Shrub Forb Forb Forb Forb Forb Forb Forb Forb Forb Forb Average Wet Average Average Average Average Dry Average Average Dry Average Average Wet Average Dry Average Average Wet Average Dry Wet Average Average Plants listed in 2005 bloom order. 2005 bloom period is indicated by letters: e ⫽ early (MayÐJune), m ⫽ middle (July to mid-Aug.), and l ⫽ late season (mid-Aug. on). Tolerance indicates plant suitability for wet-dry environments. a Although attractive to natural enemies, these species are difÞcult to establish from seed. b Apocynum cannabinum is considered an agricultural weed and should be used with caution. c Oenothera biennis attracted large numbers of Japanese beetle in both 2004 and 2005. d Solidago speciosa may be substituted in dry environments but contained fewer natural enemies and greater pest numbers. plants and included (in order of decreasing total number) Lepidoptera, Cicadellidae, Chrysomelidae, Cercopidae, and Aphididae. Herbivore Taxa. At the order level, the relative composition of the herbivore taxa were very similar in 2004 and 2005 (Fiedler 2006). Herbivores in the order Hemiptera were the most abundant, followed by Coleoptera and Thysanoptera (Table 3). Low numbers of dipteran and orthopteran herbivores were collected at plants. Miridae, primarily composed of Lygus sp., were the most numerous herbivorous insect family (Table 3). Aphididae and Cicadellidae were also common in both years (Table 3). The most numerous coleopteran herbivores were Chrysomelidae, and Cerambycidae and Curculionidae were collected in low numbers. Scarabaeidae were almost entirely composed of Japanese beetle (Popillia japonica Newman). Lepidopteran adults were not frequently collected in samples. Only adult Lepidoptera of families known to be pest species on plants of agricultural importance were counted separately as herbivores. Larvae and any unidentiÞable adults were identiÞed to order and are counted as Lepidoptera (Table 3). Discussion From the full set of 48 ßower species, ßoral resources were available to insects from 1 May through 30 September 2004 and 4 May through 4 October 2005. The overlap in plant phenology suggests that a subset of the most attractive species can be selected for further testing and habitat manipulation. The native plants tested showed differing attractiveness to natural enemies, which has also been found with exotic plants in other studies (Baggen et al. 1999, Colley and Luna 2000, Ambrosino et al. 2006). Three widely used exotics (L. maritima, F. esculentum, and V. faba) were very attractive to natural enemies, indicating that recommendations for their use are well founded. However, many Michigan native plants were as, or more, attractive as these frequently recommended exotics. The native perennials became more attractive to natural enemies as they matured and were more likely to attract more natural enemies than exotic annuals in year 2. This suggests that as perennial natives establish they have potential to be more attractive to natural enemies than previously tested annuals for habitat management (Orr and Pleasants 1996, Nentwig et al. 1998). In addition, the perennial plants tested have the potential to provide plant resources over a greater part of the growing season than annuals. Perennial natives began blooming in early May; for example F. virginiana bloomed in mid-May, followed by Z. aurea in early June. Both provide ßoral resources before any of the seeded annual plants bloomed in our study, and F. virginiana even provided ßoral resources before the danger of frost damage to annual plugs had passed. Other perennial species bloomed through September in both 2004 and 2005, during which time the only blooming exotic was L. maritima. Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Bloom 760 ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 4 In addition to nectar and pollen, perennial plants may provide a moderated microclimate and shelter from disturbance in highly disturbed agricultural areas, characteristics that have been shown to increase natural enemy effectiveness (Dyer and Landis 1996). Rebek et al. (2005) found that plants with ßowers intact did not attract signiÞcantly different numbers of natural enemies than plants with ßowers excised. Likewise, we collected natural enemies in grass alone, indicating that it may provide some beneÞt, such as moderated microclimate, shelter, and alternate prey. However, we did have a set of native plants that were signiÞcantly more attractive to natural enemies than the background grass matrix, and which could provide additional sugar and protein sources to natural enemies. We did not see alternate prey in large numbers on any plants with the exception of V. faba, which was infested with aphids in 2005, leading to a high density of lady beetle larvae, pupae, and adults on this species. Considering bloom period and attractiveness to natural enemies, we propose a set of plants most suitable for further study (Table 4). In agricultural settings, these plants could be established in strips in or along crop Þelds to provide nectar and pollen to natural enemies and evaluate the effect of strips on crop yield. In addition to attractiveness to natural enemies, the number and type of herbivore collected at a plant must be evaluated. If an herbivore occurs in higher numbers Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 4. Early season mean number of natural enemies (positive y-axis) and herbivores (negative y-axis) collected per 1-m2 plot the week before, during, and after peak bloom in (a) 2004 and (b) 2005. Plants listed in bloom order. Grass control samples were collected in 2005 from 21 June onward. Cross-hatched bars are exotic plant species. August 2007 FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS 761 at a ßowering plant than in grass alone, its pest potential in crops surrounding the ßowering plant strip must be considered (Winkler 2005). For example, Japanese beetle attraction by resource plants may be of great concern in fruit crops. The native O. biennis and exotic F. esculentum attracted large numbers of Japanese beetle in both 2004 and 2005. The presence of Lygus and Cicadellidae will be of concern to farmers of crops susceptible to direct damage or viruses transmitted by these insects. The natives V. stricta and R. pinnata attracted large numbers of Lygus in 2005. Surprisingly, samples from the previously recommended exotics C. sativum and F. esculentum also contained Lygus in relatively large numbers. In addition, the Chrysomelidae common at L. maritima included Phyl- lotreta striolata (F.), a known herbivore of cabbage and mustard, and Phyllotreta spp., a potential herbivore on brassicas. This indicates that frequently recommended exotic L. maritima attracts a known canola pest and potential pest on other Brassicas, which may increase herbivory if planted near brassicaceous crops. In native prairie and savanna habitats, grasses were a component of the plant matrix and may be vital components of habitat strips. Although not tested in our study for attractiveness to natural enemies, we planted Panicum virginicum L., Elymus canadensis L., and Schizachyrium scoparium (Michx.) Nash to test survivorship and growth in our Þeld plots. The grasses survived and Þlled the 1-m2 test plots after 2 yr of Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 5. Midseason mean number of natural enemies (positive y-axis) and herbivores (negative y-axis) collected per 1-m2 plot the week before, during, and after peak bloom in (a) 2004 and (b) 2005. Plants listed in bloom order. Grass control samples were collected in 2005 only. Cross-hatched bars are exotic plant species. 762 ENVIRONMENTAL ENTOMOLOGY Vol. 36, no. 4 growth. These species, as well as Andropogon gerardii Vitman and Sorghastrum nutans L. Nash, are all relatively easy to establish native grasses for potential inclusion with forbs in a planted strip. In addition to providing structural support, grasses have been shown to support ground beetle populations in previous studies (Lee et al. 2001, Varchola and Dunn 2001). We collected higher numbers of Nabidae and Staphylinidae in the exotic grass control than in many ßowering plant samples, indicating that these groups may also beneÞt from the inclusion of grass in plant mixtures. The natural enemy groups most frequently collected at plants for habitat management in this study could impact a variety of crop pest populations (Fiedler 2006). The most common natural enemy col- lected, Orius insidiosus, is predaceous on a variety of small, soft-bodied insects, including aphids, whiteßies, thrips, spidermites, lepidopteran eggs, and some chrysomelid beetles. The two Cantharidae species collected were Chauliognathus marginatus Fabricius and C. pennsylvanicus Deg. In their larval stage, both species are predators on soil-dwelling soft-bodied insects and have been seen feeding on adult Chrysomelidae and Cicindelidae. Both species feed exclusively on pollen and nectar as adults. The coccinellid species collected in this study included Harmonia axyridis Pallas, Coccinella septempunctata L., Coleomegilla maculata DeG., and Hippodamia variegata Goeze. All of these species are known predators on aphids and other small soft-bodied insects as larvae and adults. Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 Fig. 6. Late season mean number of natural enemies (positive y-axis) and herbivores (negative y-axis) collected per 1-m2 plot the week before, during, and after peak bloom in (a) 2004 and (b) 2005. Plants listed in bloom order. Grass control samples were collected in 2005 only. Cross-hatched bars are exotic plant species. August 2007 FIEDLER AND LANDIS: HABITAT MANAGEMENT WITH NATIVE PLANTS other plants such as Rudbeckia hirta L. and Eupatorium maculatum L. are readily available and similar to some of our highly attractive species. These species would be good candidates for broadening future native plant selection for habitat management. The establishment time of perennial plants greatly increases time before ßowering, and therefore, time before insect abundance at plants can be measured. Although perennials outperformed annual exotics that were previously recommended for habitat management in their third growing season, the perennial planting approach needs a project duration of multiple years. This difÞculty is likely one of the primary reasons that perennial plants have not been frequently considered in habitat management studies in the past. Overall, the frequently recommended exotic annual plants used in this study were highly attractive to natural enemies, but our results indicate that equal or greater numbers of natural enemies are found at some native perennial plant species compared with the exotic annuals. Not only did plants differ in the total number and type of natural enemies attracted to them, they also differed in the number and type of herbivores they attracted. Similar to Baggen et al. (1999), our study suggests the potential to grow speciÞc plant species to attract natural enemies of the pests that are most common in surrounding crops, while not providing resources to crop pests themselves. The process of screening individual plant species for their attractiveness to natural enemies allows selection of only the best plants for multiple species Þeld trials. With this information, a community of native plant species can be developed to attract insects across taxa and provide nectar and pollen throughout the season. Acknowledgments Two anonymous reviewers provided helpful comments on this manuscript. We thank D. Richards and E. Knoblock for Þeld research assistance; G. Parsons, J. Steffen, and B. Nessia for insect identiÞcation assistance; D. Sebolt and all undergraduate research assistants in the Landis laboratory who helped with plant establishment and maintenance; J. Tuell for providing formatting for Table 1; B. Schneider and Wildtype Design, Native Plants and Seed for providing plant expertise; and R. Tempelman and X. Huang for statistical assistance. This study was funded by a Michigan State University Plant Sciences Fellowship, an MSU Sustainable Agriculture: Production and Food Ecology Systems grant and USDA NC SARE Project LCN 04 Ð249. References Cited Ambrosino, M. D., J. M. Luna, P. C. Jepson, and S. D. Wratten. 2006. Relative frequencies of visits to selected insectary plants by predatory hoverßies (Diptera: Syrphidae), other beneÞcial insects, and herbivores. Environ. Entomol. 35: 394 Ð 400. Baggen, L. R., and G. M. Gurr. 1998. The inßuence of food on Copidosoma koehleri (Hymenoptera: Encyrtidae), and the use of ßowering plants as a habitat management tool to enhance biological control of potato moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). Biol. Control 11: 9 Ð17. Downloaded from https://academic.oup.com/ee/article/36/4/751/465441 by guest on 05 March 2024 The most numerous Chalcidoidea collected at resource plants was Encrytidae Copidosoma. This genus is known to contain polyembryonic parasitoids of Lepidoptera, and C. floridanum is a known parasitoid of cabbage looper (Pieris rapae L.). The Miridae collected were Plagiognathus politus Uhler and Chlamydatus associatus Uhler; both species were observed preying on soybean aphid in Michigan (Costamagna and Landis 2007). In addition, P. politus is a documented predator on the Chrysomelid Galerucella calamariensis L. Although G. calamariensis is an herbivore for weed biocontrol, P. politus may feed on other Chrysomelids that are crop pests. The natural enemy community at these native plant species, therefore, has potential to control a range of pest species, including a variety of Aphididae, thrips, herbivorous mites, Lepidoptera, and Chrysomelidae. In 2004, arthropod sampling time was limited to 30 s/1 m2 plot, whereas in 2005, sampling was continued in each plot until all ßowers were sampled. Sample duration in 79% percent of samples taken in 2005, however, was ⬍30 s. Most samples of ⬎30 s were taken from August on. Although the increased sampling time was unlikely to affect results from small plants with few ßowers, it may have increased the number of natural enemies at the largest, late blooming plants in late season 2005. Therefore, it is likely that results from 2005 indicate closer to a true estimate of insect numbers at ßowers in late 2005 than they would have had we limited sampling to 30 s. Arthropods in this study were collected by vacuum sampling, which likely biased samples toward more sedentary groups, such as arachnids. In contrast, the vacuum sampling method may have been less likely to collect more vagile natural enemy groups such as Syrphidae, as well as herbivore groups such as Lepidoptera. Rebek et al. (2005) performed arthropod sampling with both sticky cards and vacuum sampling and observed lower numbers of arachnids and higher numbers of syrphids in sticky card samples than in vacuum samples. The standardized midday sampling time provided consistency between insect samples. However, crepuscular and nocturnal insect groups, including Chrysopidae (Duelli 1984) and Arachnida (Foelix 1996), may have been underrepresented. In this study, we did not assess whether natural enemy insects were actually feeding on plant nectar and pollen or using the plant for other resources, such as alternate prey or favorable microclimate. Future research could determine which natural enemy and herbivore species beneÞt from plant resources provided by each plant species, as well as whether natural enemies found at resource plants forage in adjacent crops. 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