Native Habitat Restoration, Sustainable IPM and Beneficial Insect Conservation

Attraction of beneficial insects to flowering plants

More than 4,000 sticky traps were deployed on 103 species of flowering perennial plants during April-November 2011-13. Analyses of data from this three-year period resulted in the rankings of plant species attractivity to beneficial insects (Table 2). All groups of beneficial insects (Table 1) were combined to create these rankings.

Sagebrush (Artemisia tridentata) (Photo 2) was ranked #1 in the number of beneficial insects attracted, but most of these insects were parasitic wasps. Sagebrush flowers in October when there is little other nectar available, and this may have been a factor in the attractivity of this plant. However, sticky-trapping during non-flowering periods (spring-summer) also showed significant attraction to beneficial insects.

The second-ranked plant for attraction to beneficial insects was Spreading Dogbane (Apocynum androsaemifolium), and this plant attracted a great diversity of beneficial insects. In contrast, the # 3 plant, Slender Hawksbeard (Crepis atribarba) attracted primarily beneficial flies similar to the # 5 plant Oregon Sunshine (Eriophyllum lanatum)(Photo 3). The # 4 and # 6 plants (Sunflower, Yarrow) attracted a wide diversity of beneficial insects (Photos 4).

The buckwheat genus Eriogonum was the most successful group of plants in attracting beneficial insects. Ten species of buckwheat are ranked in the top 67 beneficial insect-attracting plant species:

Beneficial Insects Attracted to Flowering Buckwheats, Eriogonum spp.

Buckwheats (Eriogonum spp.) comprise a group of attractive perennial desert shrubs that thrive in the shrub-steppe of central Washington. All produce masses of yellow, white or sometimes pinkish flowers that appear from casual observation to be attractive to a range of insects. Some are spring-flowering, others bloom in the summer, and a few flower in the autumn. Ten species occur in or near the Columbia Basin and would be candidates for restoration in vineyards if shown to have benefits for attracting and sustaining insect predators, parasitoids and pollinators. These buckwheat species are also larval hosts for at least 11 species of lycaenid butterflies (James and Nunnallee 2011). Information on the insect fauna attracted to the flowers of Eriogonum is limited. Cockerell (1901) reported on bees visiting two Eriogonum species in southern California, while Tepedino et al. (2011) concluded that insect pollinators visiting blooms of a rare Eriogonum species in Colorado were abundant and diverse. Morandin et al. (2011) found the greatest number of beneficial insects (predators and parasitoids) occurred on California Buckwheat (Eriogonum fasciculatum Benth.) when compared to five other native flowering plants in central California. No information is available on insects attracted to Eriogonum spp. in the Pacific Northwest. Here we report the results of a field study on the attraction of beneficial insects to 10 species of Eriogonum in central Washington.

This study was conducted over two seasons (2011, 2012) in the Yakima Valley of central Washington by identifying and counting beneficial insects attracted to blooming native buckwheat, Eriogonum spp., using transparent sticky traps. Nine species, Eriogonum elatum Douglas ex Benth. (Tall buckwheat), E. compositum Douglas ex Benth. (Arrowleaf buckwheat), E. niveum Douglas ex Benth. (Snow buckwheat), E. thymoides Benth. (Thymeleaf buckwheat), E. douglasii Benth. (Douglas’ buckwheat), E. sphaerocephalum Douglas ex Benth. (Rock buckwheat), E. strictum Benth. (Blue Mountain buckwheat), E. heracleoides Nutt. (Parsnip flowered buckwheat), and E. microthecum Nutt. (Slender buckwheat) were located growing naturally in shrub-steppe habitats at eight locations near irrigated agriculture along the Yakima Valley. A tenth species, (E. umbellatum Torr. (Sulphur flower buckwheat)), was included in two plot plantings of Eriogonum spp. (which also included E. sphaerocephalum, E. niveum, E. heracleoides, E. douglasii, and E. thymoides) established in 2009 and 2011 at the Washington State University Irrigated Agriculture Research and Extension Center (WSU-IAREC) at Prosser, WA. Despite location in an agriculturally developed area, the latter site is close (1-3 km) to shrub-steppe habitat. Transparent sticky traps (WindowBugCatcher, large 40.6 x 12.1 cm, Alpha Scents Inc., Portland, OR) were used, avoiding trap color as a potential influence on insect attraction. Traps were attached to plants as soon as blooming commenced. At each site and on each occasion trapping was conducted, three traps were placed on three plants of each Eriogonum species. During the two seasons traps were placed on 21-69 plants of each species with the exception of E. microthecum for which only nine plants were used (Table 3). Short bloom periods reduced trapping opportunities for E. thymoides, and E. douglasii. Plants with traps were at least 5 m from other plants/traps at natural sites, and there was at least 3 m separation in the WSU-IAREC plots. In the WSU-IAREC plot plantings, 15 plants of each species were grown in 2 x 1m plots with three replicates. Traps were attached to plants using flexible wires and positioned to provide a sticky surface immediately above or adjacent to the flowers. Traps were left in place for 12-14 days before removal and were replaced if blooming continued. Bloom period data were compiled for each species. In a few instances follow-up trapping occurred on the same plants (when plant numbers were limited), but usually different plants were chosen. Traps collected from the field were transported to the laboratory and stored at -30 ºC until examined under a stereomicroscope. All insects were identified to family or species and counted. The incidence and abundance of 34 species, genera or groups of winged beneficial insects were recorded (Table 1). Numbers of the grape leafhopper pests, Erythroneura spp. were also recorded. Beneficial insects were condensed into 10 categories: Lacewings (Chrysopidae, Hemerobiidae), Ladybeetles (Coccinellidae), predatory true bugs (Miridae, Anthocoridae, Nabidae), predatory thrips (Aeolothripidae), predatory and parasitic flies (Syrphidae, Empididae, Dolichopodidae, Tachinidae), ichneumonid and braconid wasps (Ichneumonidae, Braconidae), Anagrus wasps (Mymaridae), Coccophagus and Metaphycus wasps (Aphelinidae, Encyrtidae), other parasitic wasps (Pteromalidae, Eulophidae, Trichogrammatidae, Scelionidae) and bees (Apoidea). Bumblebees and larger wasps such as yellow jackets and hornets were often able to extricate themselves from the sticky material and were rarely trapped. Trapping data were log (log x) transformed prior to analyses to improve normality of variances and then back-transformed for reporting. Repeated measures ANOVA with means separated using the Holm-Sidak method was used for analyses (SigmaStat Version 3.0. SPSS Inc).

Beneficial insects dominated trap catches throughout this study. Very few pest insects were trapped. Aphids and grape leafhoppers (Erythroneura spp.) were occasionally encountered, although only 29 grape leafhoppers were recorded on the 402  traps examined during this study. Combining all categories of beneficial insects the mean number per trap ranged from 48.5 (E. umbellatum) to 167.7 (E. elatum) (Fig. 1). Three species (E. elatum, E. compositum, E. niveum) (Photos 5-7) attracted significantly more beneficial insects than the six species least visited by beneficial insects (F = 3.67; df = 9, 101; P < 0.001) (Fig. 1). Eriogonum niveum attracted greatest numbers of bees and parasitic wasps and E. elatum was most attractive to predatory and parasitic flies and predatory true bugs (Fig. 1). Eriogonum compositum was most attractive to ichneumonid and braconid wasps (Fig. 1). Eriogonum microthecum, E. douglasii, E. thymoides and E. umbellatum generally attracted fewer beneficials than the other species. There were no significant differences among Eriogonum species in their attraction of lacewings, ladybeetles, thrips, Anagrus or Coccophagus spp./Metaphycus spp. (P > 0.05) (Table 4).

The bloom periods of the 10 Eriogonum species in this study extended from mid-April to the end of September and ranged from four to five weeks (E. douglasii, E. thymoides) to almost three months (E. elatum, E. microthecum) (Table 5).

Eriogonum spp. commonly known as ‘wild buckwheats’ comprise one of the largest genera of plants found in North America north of Mexico. More than 253 species occur from the islands off the California coast to the coastal plains of South Carolina, Georgia and Florida and from the Alaska and Yukon area in the north to the Mexican border. Elsewhere the genus is confined to the trans-volcanic ranges of central Mexico and to areas of northern Baja California. Within the context of flowering plants with potential to attract and sustain populations of beneficial insects, the common name ‘buckwheats’ for Eriogonum spp. is unfortunate. In pest management literature, ‘buckwheat’ usually refers to Fagopyrum esculentum (Moench), a crop plant cultivated for its grain-like seed (Neskovic et al. 1986). It is also used as a cover crop or ground cover effective in attracting and sustaining beneficial insects and is commonly used to enhance conservation biological control of crop pests (Stephens et al. 1998). Eriogonum and Fagopyrum are both in the Family Polygonaceae and our study suggests Eriogonum spp. share with F. esculentum the attribute of attracting beneficial insects. Fagopyrum esculentum has one of the highest moisture requirements of any cereal (Neskovic et al. 1986) and its use as a ground cover in arid regions like central Washington is impossible without supplemental irrigation. In contrast, Eriogonum spp. are drought-tolerant (Meyer and Paulsen 2000), flowering during spring-fall with minimal or no rainfall. Using native rather than exotic flowering plants as ground covers or beneficial insect refugia for enhancement of conservation biological control in agriculture, is clearly preferable in terms of optimal functional linkages with the local insect fauna. Native predators, parasitoids and pollinators should respond optimally to native flora.

This study confirms anecdotal observations that wild flowering buckwheats appear to attract a diversity and abundance of beneficial insects in central Washington. Arthropods (e.g. aphids, mites) that serve as prey to many of the attracted predators were rarely seen feeding on buckwheats and appear unlikely to have influenced attraction. A number of the predators and parasitoids attracted to Eriogonum spp. are important in biological control of wine grape pests in central Washington. For example, lacewings, ladybeetles, predatory true bugs and thrips prey on important grape pests such as leafhoppers, mites, thrips and mealybugs. Parasitoids (Mymaridae, Encyrtidae, Aphelinidae) help regulate populations of leafhoppers, scale insects and mealybugs on Washington grapes (James 2013). The 10 Eriogonum spp. evaluated in this study varied significantly in terms of numbers of beneficial insects attracted. Combining numbers of all the beneficial insects included in this study, three species (E.elatum, E. compositum and E. niveum) were significantly more attractive averaging more than 150 individuals per trap. At the other end of the scale, E. thymoides, E. sphaerocephalum, E. douglasii, E. umbellatum and E. microthecum averaged around 50 individuals per trap. However, even 50 beneficial insects per trap is indicative of a reasonably attractive flowering plant. Sticky-trapping (same protocols) of Medicago sativa L. (Alfalfa), considered highly attractive to beneficial insects (Elliot et al. 2002), at site 4 in July 2011 yielded a mean of 46.3 beneficial insects per trap (James, Seymour, Lauby, Buckley, unpubl.). This suggests that even the poorest performing Eriogonum spp. are comparable to the highly-rated M. sativa in attracting beneficial insects. Other differences between Eriogonum spp. were evident when different groups of beneficials were considered. Eriogonum elatum was significantly more attractive to beneficial Diptera and Heteroptera than the other buckwheats. The anthocorid Orius tristicolor (White) was the dominant predatory bug found on E. elatum traps and empidid flies dominated the dipteran fauna. Most Eriogonum spp. attracted high numbers of primarily native bees. Honey bees generally made up only about 10% of bees trapped. Parasitic wasps including ichneumonids and braconids were highly attracted to E. compositum and E. niveum. Numbers of other beneficial insects were generally low (< 5/trap) and did not differ among buckwheat species. The relatively low ranking of E. umbellatum is surprising as the blooms of this species are often covered with beneficial insects at some locations, for example in central Oregon (D.G.J., unpublished data). This species is recognized as having a number of subspecies or varieties (Reveal 1968) and these may differ in beneficial insect attraction.

This study provides compelling evidence that perennial flowering wild buckwheats in central Washington are highly attractive to a range of beneficial insects including predators, parasitoids and pollinators. Consequently, they offer great potential as plants that could be cultivated within or around crops with the aim of luring and sustaining natural enemies of pest arthropods. In organic or low pesticide input crops this would enhance conservation biological control and more importantly, increase sustainability. Viticulture in central Washington is a good example of an agroecosystem that is based on minimal pesticide inputs and biologically-based pest control. Wild buckwheats with their attraction to beneficial insects appear to be excellent candidates for use in viticulture habitat restoration strategies that are intended to improve and sustain conservation biological control. All of the Eriogonum spp. in this study are relatively low growing (20-50 cm), except E. microthecum (1-1.5 m) and E. elatum (1-2 m) (Turner and Gustafson 2006), and could be cultivated within vineyard rows. Bloom periods of the 10 Eriogonum spp. in this study ranged from early spring to fall, providing opportunities for multi-species plantings and prolonged blooming.

Wild buckwheats possess another ecosystem service attribute. They are larval hosts to a large number of lycaenid butterflies (blues, coppers, hairstreaks and metalmarks). In Washington they host at least 11 species (Pyle 2002, James and Nunnallee 2011). Populations of many of these small but charismatic butterflies are declining particularly in agricultural and urban development areas, primarily due to destruction of habitat and host plants. Reintroducing Eriogonum spp. to crop lands such as vineyards has the potential to improve and sustain populations of these butterflies. Combining biologically-based pest management strategies in viticulture with butterfly conservation is a concept that is already becoming a reality in Europe and New Zealand (Schmitt et al. 2008, Gillespie and Wratten 2012). Wild buckwheats with the dual attributes of hosting a large number of vulnerable butterfly species and attracting pollinators and natural enemies of pests, could become a cornerstone plant group for viticultural programs integrating pest management and butterfly conservation in the western United States.

Ballard, M., J. Hough-Goldstein and D. Tallamy. 2013. Arthropod communities on nonnative early successional plants. Environ. Entomol. 42: 851-859.

Cockerell, T. D. A. 1901. Bees from southern California visiting flowers of Eriogonum and Rhus. Can. Emtomol. 33: 281-283.

Elliot, N. C., R. W. Kieckhefer, G. J. Michels Jr., and K. L. Giles. 2002. Predator abundance in alfalfa fields in relation to aphids, within-field vegetation and landscape matrix. Environ. Entomol. 31: 253-260.

Fiedler, A. K., and D. A. Landis. 2007. Attractiveness of Michigan native plants to arthropod natural enemies and herbivores. Environ. Entomol. 36: 751-765.

Fiedler, A. K., D. A., and S. Wratten. 2008. Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol. Control 45: 254-271.

Frank, S. D., P. M. Shrewsbury and O. Esiekpe. 2008. Spatial and temporal variation in natural enemy assemblages on Maryland native plant species. Environ. Entomol. 37: 478-486.

Gillespie, M. and S. D. Wratten. 2012. The importance of viticultural landscape features and ecosystem service enhancement for native butterflies in New Zealand vineyards. J. Insect Conserv. 16: 13-23.

Goulson, D., G. C. Lye, and B. Darvill. 2008. Decline and conservation of bumble bees. Annu. Rev. Entomol. 53: 191-208.

Isaacs, R., J. Tuell, A. Fiedler, M. Gardiner, and D. Landis. 2009. Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. Front. Ecol. Environ. 7: 196-203.

Hodgson, J. A., W. E. Kunin, C. D. Thomas, T. G. Benton and D. Gabriel. 2010. Comparing organic farming and land sparing: optimizing yield and butterfly populations at a landscape scale. Ecol. Lett. 13: 1358-1367.

James, D. G. (2013).Beneficial Arthropods pp. 49-64. In Field Guide for Integrated Pest Management in Pacific Northwest Vineyards PNW Extension Pub. PNW644 (eds. M. Moyer and S. D. O’Neal.

James, D. G., and D. Nunnallee. 2011. Life Histories of Cascadia Butterflies. Oregon State University Press., Corvallis, OR.

James, D. G., L. S. Seymour, G. Lauby and K. Buckley. 2013. Beauty with benefits: naturescaping Washington vineyards to sustain biological control and provide butterfly habitat. Proc. 4^th Int. Symp. Biol. Cont. Arth. Pucon, Chile pp. 195-197.

Landis, D. A., S. D. Wratten, and G. M. Gurr. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 43: 175-201.

Meyer, S. E., and A. Paulsen. 2000. Wild buckwheat (Eriogonum Michx. (Polygonaceae)). Native Plants J. 1: 18-24.

Morandin, L., R. F. Long, C. Pease, and C. Kremen. 2011. Hedgerows enhance beneficial insects on farms in California’s central valley. Calif. Agric. 65: 197-201.

Neskovic, M., V. Srejovic, and R. Vujicic. 1986. Buckwheat (Fagopyrum esculentum Moech). Biotech. in Agric. and Forest. 2: Crops 1: 579-602.

New, T. R., R. M. Pyle, J. A. Thomas, C. D. Thomas and P. C. Hammond. 1995. Butterfly conservation management. Annu. Rev. Entomol. 40: 57-83.

Pisani Gareau, T. L., D. K. Letourneau, and C. Shennan. 2013. Relative densities of natural enemy and pest insects within California hedgerows. Environ. Entomol. 42: 688-702.

Pyle, R. M. 2002. The Butterflies of Cascadia: a field guide to all the species of Washington, Oregon and surrounding territories. Seattle Audubon Society. 420p.

Reveal, J. L. 1968. Some nomenclatural changes in Eriogonum (Polygonaceae). Int. Assoc. for Plant Tax. 17: 531-533.

Schmitt, T., B. Augenstein and A. Finger. 2008. The influence of changes in viticulture management on the butterfly (Lepidoptera) diversity in a wine growing region of southwestern Germany. Eur. J. Entomol. 105: 249-255.

Stephens, M. J., C. M. France, S. D. Wratten and C. Frampton. 1998. Enhancing biological control of leafrollers (Lepidoptera: Tortricidae) by sowing buckwheat (Fagopyrum esculentum) in an orchard. Biocon. Sci. Tech. 8: 547-558.

Tepedino, V. J., W. R. Bowlin, and T. L. Griswold. 2011. Diversity and pollination value of insects visiting the flowers of a rare buckwheat (Eriogonum pelinophilum: Polygonaceae) in disturbed and “natural” areas. J. Pollination Ecol. 4:57-67.

Turner, M. and P. Gustafson. 2006. Wildflowers of the Pacific Northwest. Timber Press, Portland, Oregon. 511 pp.

Pest and Natural Enemy Populations in Habitat-Enhanced and Conventional Vineyards

Commercial wine grape vineyards were cooperators in this multi-season (2011-13) study which commenced in spring 2011. A pair of vineyards was identified and selected in each of the Columbia Gorge, Columbia Basin (Wahluke Slope), Walla Walla Valley and Yakima Valley (Red Mountain) viticultural areas. Each pair consisted of a ‘native habitat-enhanced’ (VH) and a ‘native habitat-reduced’ or conventional (C) vineyard. Habitat-enhanced vineyards are situated close to natural areas with current management practices designed to maximize colonization of native plants in and/or around grape plants. Habitat-reduced vineyards are situated away from natural areas and colonization of native plants has not been encouraged and may have been actively discouraged. Monitoring of pest and beneficial insect and mite populations commenced in all vineyards in May of each year, continuing at two-weekly intervals until September. On each visit leaf samples were taken from grapevines and sticky yellow traps were placed in the vineyard. Leaves were examined in the laboratory for pests and beneficials as were sticky traps. Additional sticky traps were placed in native habitats present adjacent to the habitat-enhanced vineyards.

2011 Vineyard pairs in the Columbia Gorge (CG) and Wahluke Slope (WS) areas showed the greatest contrast in terms of numbers of native plant species present close to grapevines and data from these sites are presented (Photos 8 & 9). In both areas, the VH vineyard had a diverse immediate area flora that conservatively contained at least 30 native species occurring at medium-high density. In contrast, the C vineyards in both areas had a low-diversity flora comprising only 7-12 species.

Pest incidence/abundance. Spider mite populations were absent (WS) or occurred at very low density (CG). However, populations were significantly greater in the C vineyard than in the VH vineyard at CG (Fig. 2). Predatory and mildew-feeding mites (tydeids) were commoner in the CG VH vineyard along with rust mites, although the latter were substantially below levels likely to cause economic damage (Fig. 2). Leafhoppers were virtually absent in the CG vineyards but adults were common (mean 30 +/trap) in the WS VH vineyard. However, this high level of adults did not translate into economically damaging levels of nymphs on leaves (Fig. 3). Very few leafhoppers were seen at the WS C vineyard due to spray application.

Beneficial insect incidence/abundance. Data on abundance of four groups of beneficial insects in VH and C vineyards at WS and in the CG are shown in Figs. 4-5. Abundances in native habitat (H) areas close to the VH vineyard are also shown. In most cases greater populations of beneficials occurred in the native habitat area (H) alongside the VH vineyard than in the C and VH vineyards. In a number of cases (e.g. predatory beetles and bugs, lacewings (WS only), parasitic wasps), beneficial insect populations were greater in the VH than in the corresponding C vineyard, suggesting dispersal from the adjacent habitat into the vineyard. However, with some groups of beneficials (e.g. beneficial flies, lacewings (CG)), there appeared to be no movement from habitat into the adjacent vineyard (Figs. 4-5).

2012 In 2012, an additional habitat-enhanced vineyard was monitored in the Columbia Basin and Walla Walla areas. Each area had one or two ‘native habitat-enhanced’ (VH) and a ‘native habitat-reduced’ (C) vineyard. Habitat-enhanced vineyards are situated close to natural areas with current management practices designed to maximize colonization of native plants in and/or around vineyards. Habitat-reduced vineyards are situated away from natural areas and colonization of native plants has not been encouraged and usually actively discouraged. Monitoring of pest and beneficial insect and mite populations commenced in all vineyards in May, continuing at two-weekly intervals until September. On each visit leaf samples were taken from grapevines and sticky yellow traps were placed in the vineyard. Leaves were examined in the laboratory for pests and beneficial insects and mites as were sticky traps. Additional sticky traps were placed in native habitats present adjacent to the habitat-enhanced vineyards.

Inventories of flowering plants and butterflies were obtained for each vineyard site during fortnightly visits in 2012. As expected, the habitat-enhanced vineyard sites had greater numbers of flowering plant species than habitat-reduced sites Similarly, most habitat-enhanced vineyards appeared to support greater numbers of butterflies, both in abundance of individuals and species diversity (see later section on pollinator conservation). .

Beneficial insect abundance as determined by sticky trapping was significantly greater at habitat-enhanced than habitat-reduced vineyard sites (Fig. 6).

This trend was evident in all major beneficial insect groups when examined separately including the important grape leafhopper parasitoids, Anagrus spp. (Fig. 7).

Examination and analysis of beneficial insect abundance and diversity in habitat areas around the habitat-enhanced vineyards, indicated that some beneficial insect groups dispersed more effectively to the vineyard than others. For example, parasitic wasp abundance was substantially greater in surrounding habitat than in 2 ‘enhanced’ vineyards at Red Mountain (Fig. 8). In contrast beneficial beetles (Photo 10) and bugs (Photo 11) in the Columbia gorge were more abundant in the habitat-enhanced vineyard than in surrounding habitat (Fig. 9).

Grape pest levels were generally low in all vineyards but there was a clear trend for greater incidence of mites, leafhoppers, mealybugs and scale insects in habitat-reduced vineyards compared to habitat-enhanced vineyards (Figure 10). The numbers of beneficial mites (predators of rust and spider mites) on leaves did not differ greatly between habitat-reduced and enhanced vineyards suggesting beneficial insects respond better to habitat improvement.

2013   Similar data on the abundance of pest and beneficial insects in habitat-enhanced and conventional vineyards were obtained in 2013. Significantly greater numbers of beneficial insects (all groups) occurred in habitat-enhanced vineyards compared to conventional vineyards (data from the 4 regions combined) (Fig. 11). However, significantly greater numbers occurred in the habitat surrounding the habitat-enhanced vineyards. Examination of specific groups showed significantly greater numbers of parasitic wasps (Fig. 12) and Anagrus spp. in habitat-enhanced compared to conventional vineyards. However, no differences in beneficial flies, native bees, predatory bugs, ladybeetles and predatory thrips were detected. All these groups (except ladybeetles and thrips) were significantly more abundant in the habitat surrounding the habitat-enhanced sites (Fig. 11-12).

On a regional basis the same trend for greater numbers of beneficial insects (habitat>habitat-enhanced>conventional), was evident at the sites in the Yakima Valley (Red Mt), and Columbia Gorge (Lyle) (Fig. 13). At Quincy (Wahluke Slope) greatest numbers of beneficials occurred in the habitat-enhanced vineyard while at Walla Walla no differences occurred in beneficial insect numbers between habitat, habitat-enhanced and conventional (Fig. 13).

Overall, leaf pest numbers (spider mites, rust mites) were greater in conventional vineyards (Fig. 14). Beneficial mites (phytoseiid predatory mites, tydeid mites) were commoner in habitat-enhanced vineyards (Fig. 14).

Butterfly Diversity and Abundance in Habitat-enhanced and Conventional Vineyards

South central Washington State in the Pacific Northwest of the United States is characterized climatically by low annual rainfall, hot, sunny summers, and cold wet winters. It is largely a basin or low plateau punctuated by dry ranges and scored by deep coulees and channeled scablands. The Columbia River runs through the region fed by other rivers such as the Snake and the Yakima. This largely treeless area is dominated by a rich and diverse shrub-steppe ecosystem that has sagebrush (Artemisia tridentata) and bunchgrass prairie as the primary vegetation. Surprisingly perhaps, this region supports a large and diverse fauna of butterflies; about half of the ~ 160 species known from the Pacific Northwest occur in south-central Washington (Pyle 2002; James and Nunnallee 2011). South central Washington is also a major agricultural production area supported by irrigation derived from annual snowpack in the nearby Cascade Mountains. More than 100 crops are grown in the region, including apples, wheat, corn, potatoes, hops and grapes. Agricultural development over the past 40-50 years has severely eroded the shrub-steppe, especially in the valleys, and many of the region’s butterflies have suffered significant declines as habitats have been lost (Pyle 1974, 2002; James and Nunnallee 2011).

The area planted to wine grapes in south central Washington has grown from a few hundred hectares in the mid-1970s to more than 13,000 hectares in 2014, and production is now only second to California in the U.S. The vast majority of these new vineyards have been planted on former shrub-steppe lands. Pest management in Washington viticulture was dominated by the widespread use of broad-spectrum insecticides up until about 2000 (Cone et al. 1990). Thereafter, there has been a consistent decline in the use of insecticides in Washington wine grapes, resulting in biologically-based integrated pest management today (James, 2013). Very few insecticides are now applied in Washington grapes and those that are, are generally narrow-spectrum and have reduced or no impact on non-target organisms. Current research on pest management in Washington wine grapes is centered on increasing the efficacy and sustainability of conservation biological control of pests by restoring native plants and habitats within and around vineyards (http://www.wavineyardbeautywithbenefits.com/). The establishment of native shrub-steppe flora on agricultural land not subjected to frequent pesticide applications opens up opportunities not only for native plant conservation but also for the conservation of insects like butterflies that are associated with these plants. The potential for Washington State wine grape vineyards to become butterfly conservation areas is explored in this field study.

Vineyard sites

A pair of vineyards (habitat-enhanced, conventional) was selected in each of four viticultural regions (Columbia Gorge (CG), Walla Walla Valley (WWV), Yakima Valley (YV), Wahluke Slope (WS)) in south-central Washington, which differ enough climatically and geologically to warrant individual appellation status (Gregutt 2007). In each region the pair of sites was separated by 0.5-32 km. Habitat-enhanced vineyards had a history of allowing plants, mostly natives, to colonize the site and/or some attempt had been made to establish native plants. The CG and WS sites had been restoring native plants for 15-20 years. The YV and WWV vineyards had only been restoring native plants for about five years. An inventory was taken of all plant species occurring at each vineyard site during the survey period. Insecticides were never (CG, WS) or only rarely used (YV, WWV). All insecticides were ‘soft’ and narrow-spectrum in their action, unlikely to have major deleterious effects on butterfly populations. The conventional vineyard sites had made no attempt to encourage native plants and frequently used herbicides within vine rows. Native plants were also not encouraged in areas outside the grapevine block. Insecticides were occasionally used in the conventional vineyards (one to two sprays/season), but all were narrow spectrum.

Butterfly surveys

Butterfly surveys were conducted at each vineyard during May to September in 2012 and 2013. Vineyards were visited every two weeks, and the number and species of butterflies seen during a 30-40 minute period between 1000h and 1500h were recorded. In most instances butterflies were identified in the field and verified by photographs. Some species were netted to confirm identity. Surveying was conducted in the vineyard and the immediately surrounding area up to 25 m from the grapes. Weather on most occasions was sunny and warm (15-38 ºC) and conducive to butterfly activity.

The habitat-enhanced vineyard sites supported a significantly greater number of plant species (mean 47.0 ± 6.3, range 32-61) than conventional vineyard sites (mean 8.7 ± 4.1, range 4-21, t = 5.071, 6 df, P = 0.002) (Tables 6-10). Similarly, a mean of 30.2 ± 3.3 native plant species were present in habitat-enhanced vineyards compared to 5.0 ± 1.7 in conventional vineyards (t = 6.774, 6 df, P < 0.001). Habitat-enhanced vineyards had a significantly greater number of plants known to be visited by butterflies for nectar (42 ± 2.1) compared to 8.0 ± 4.0 plants in conventional vineyards (t = 5.889, df = 6, P = 0.001). Habitat-enhanced vineyards supported a significantly greater number of known butterfly larval host plants (17.0 ± 2.2) than conventional vineyards (3.5 ± 2.5. t = 4.086, df = 6, P = 0.006).

Twenty-nine butterfly species were recorded from habitat-enhanced vineyards, with only 10 of these recorded from conventional vineyards (Table 11). Of the 10 species found in conventional vineyards, six are widespread, mobile, wide-ranging species that may not have been resident in the vineyards. Twenty of the 29 species recorded in habitat-restored vineyards are likely to be resident in the vineyard or adjacent areas (Table 11). Overall, there were double the number of species in habitat-enhanced vineyards (5.62 ± 1.46) compared to conventional vineyards (2.75 ± 0.75) (t = 1.749, df = 14, P = 0.1). A significantly greater number of species occurred in the CG and WWV habitat-enhanced vineyards (16.0 ± 1.0) compared to the conventional vineyards (6.0 ± 1.0, t = 7.071, df = 2, P = 0.019) in these regions. Smaller numbers of butterfly species (three to six) occurred in YV and WS vineyards, and although there was no difference in numbers between habitat-enhanced (three) and conventional sites (three) at WS, twice as many (six) species occurred at the YV habitat-enhanced site than in the conventional vineyard (three).

Butterfly abundance was significantly greater in habitat-enhanced vineyards (20.37 ± 4.88 individuals/visit compared to conventional vineyards (5.5 ± 1.74 (Mann Whitney Rank Sum Test T = 88, P = 0.038) (Fig. 15). Differences were greatest at the CG and WWV vineyards (t test = 5.596, df = 6, P = 0.001) and least at the YV and WS vineyards (Mann Whitney Rank Sum Test T = 22. P = 0.343) (Fig. 15).

Butterfly populations have rarely been studied in vineyards. Shmitt et al. (2008) working in Germany reported that butterfly abundance and diversity were much lower in vineyards than in nearby fallow land, ascribing this to a lack of nectar and host plant resources in vineyards as well as negative effects from pesticide applications. Low butterfly abundance and diversity was also reported from vineyards in New Zealand, but this was largely a consequence of the small number of butterflies (23 spp.) resident in New Zealand (Gillespie and Wratten, 2012). However, native plants established in New Zealand vineyards were not associated with increased abundance and/or diversity of butterflies (Gillespie and Wratten, 2012).

In contrast, our study suggests that the pest management enhancement strategy of restoring native plants and habitats in a low pesticide-input crop like wine grapes in central Washington, may have substantial benefits for butterfly abundance, diversity and conservation. Many flowering native plants attractive to natural enemies of pest insects in central Washington are also important nectar sources or larval host plants for butterflies. For example, 10 species of native flowering buckwheats (Eriogonum spp.) were shown to be attractive to a wide range of beneficial insects in central Washington (James et al. 2014). These plants are also larval hosts to at least 11 lycaenid butterflies (James and Nunnallee, 2011) (Photo 13).

The aim of this study was to compare butterfly abundance and diversity in wine grape vineyards that actively encourage or restore native plants and vineyards that follow a conventional approach of minimizing and discouraging establishment and growth of plants other than grapevines. There were 2-13 X as many plant species at habitat-enhanced sites as at conventional sites, with most of these plants known nectar resources for butterflies. More than a third of plant species at habitat-enhanced sites are known to host larvae of Washington butterflies. Butterfly diversity and abundance was demonstrably greater in habitat-enhanced vineyards in three of the four areas. The greatest differences occurred in the CG and WWV appellations. The habitat-enhanced vineyard in the CG has been under the current management since 1994 and had the greatest butterfly diversity with 21 species. The WWV vineyard has a shorter history of habitat enhancement (~ 5 years) but has an aggressive program of establishing flowering native plant species. Thirteen butterfly species were recorded at this site. The YV habitat-enhanced vineyard has only recently begun establishing native plants and only six butterfly species were recorded. The WS habitat-enhanced vineyard has been encouraging native plants for 20 years but is in a hotter and drier appellation, which may explain the low apparent butterfly diversity (3 species). Curiously, at least three common and widespread species seen in the other habitat-enhanced vineyards (Pyrgus communis, Pholisora catullus, Heliopetes ericetorum) were not recorded at the WS vineyard, despite the presence of their host plants (Malva spp., Chenopodium).

Four of the 29 butterfly species recorded in the vineyards in this study are considered migratory or highly dispersive and can turn up almost anywhere in eastern Washington (Table 11). However, for the majority of butterfly species we found in vineyards, larval host plants were also present. For example larval host plants for 18 of the 21 species recorded in the CG habitat-enhanced vineyard were also present in or very near to the vineyard. Similarly 12 of the 13 species recorded at the WWV habitat-enhanced vineyard also had larval host plants present. Thus, there is a good possibility that breeding populations of these butterflies are present in these habitat-enhanced vineyards.

Our research on beneficial insect attraction to native plants in Washington has identified many other plant species apart from Eriogonum spp. (James et al., 2014) that have potential for enhancing pest management in wine grape vineyards and are also butterfly host and/or nectar plants (James et al., in prep.). The importance of stinging nettles (Urtica dioica) as larval hosts for a range of nymphalid butterflies (Photo 14) is well known (James and Nunnallee, 2011), but their great value in harboring predatory bugs and parasitic wasps is less well known (James et al. in prep.). In the future Washington wine grape growers should be able to select plants for establishment in vineyards based on their value to pest management and to butterfly conservation. This should enable vineyards to play an important role in butterfly conservation by creating habitat for vulnerable shrub-steppe species, as an additional benefit of minimizing pest management concerns and costs. Vineyards in different viticultural regions of Washington should be able to tailor their native vegetation mix to suit both their local pest pressures and local opportunities for butterfly conservation. For example, many new vineyards in the YV appellation, particularly around the Tri-Cities in south central Washington, occupy sites that formerly hosted populations of Plebejus icarioides (Boisduval’s blue) (Photo 15) and Chlosyne acastus (Sagebrush checkerspot) (James, unpubl. obs). In most cases, populations of these butterflies still exist within a few kilometers of vineyards and by simply restoring nectar sources and the larval host plants of these species (lupines, rabbitbrush), it should be possible to re-extend the range of these species to again include the vineyard areas.

Successful butterfly conservation within agricultural lands primarily depends on the availability of nectar and larval hosts as well the absence or near-absence of agricultural chemicals. Achieving the latter, until recently, has been difficult if not impossible in most crops and agricultural regions. However, significant advances have been made in non-chemical pest management and crops like wine grapes in Washington can be produced with no or very little pesticide input. In addition, many contemporary pesticides have apparently little or no impact on non-target organisms, although the sub-lethal impacts of these remain to be determined in many cases. Thus the situation we report here of butterflies co-existing with viticultural production in Washington is a scenario which is likely to become increasingly common in agricultural areas worldwide during the next few decades.

References

Cone WW, Wright LC, Conant MM (1990). Management of insect pest populations in a developing cool-climate grape industry. In: Monitoring and Integrated Management of Arthropod Pests of Small Fruit Crops. Intercept Ltd, Hampshire, England.

Gillespie M, Wratten SD (2012). The importance of viticultural landscape features and ecosystem service enhancement for native butterflies in New Zealand vineyards. J Insect Conserv 16: 13-23.

Gregutt P (2007). Washington wines and wineries: the essential guide. Univ. Calif. Press.

James DG (2013). Beneficial Arthropods. In: Field Guide for Integrated Pest Management in Pacific Northwest Vineyards. A Pacific Northwest Extension Publication PNW644, Washington State University.

James DG, Nunnallee DN (2011). Life Histories of Cascadia Butterflies. Oregon State University Press 447 pp.

James, DG, Seymour L, Lauby G, Buckley K (2014). Beneficial Insects Attracted to Native Flowering Buckwheats (Eriogonum Michx) in Central Washington. Environ. Entomol. (in press).

Pyle RM (1974). Watching Washington Butterflies. Seattle Audobon Society.

Pyle RM (2002). The Butterflies of Cascadia. Seattle Audobon Society.

Schmitt T, Augenstein B, Finger A (2008). The influence of changes in viticulture management on the butterfly (Lepidoptera) diversity in a wine growing region of southwestern Germany. Eur. J. Entomol. 105: 249-255.

Discussion

The outcomes from this project provide a solid foundation for strategies to develop vineyard ecosystems that enhance conservation biological control of pests while providing habitat for threatened native flora and pollinators.

The concept of restoring native habitat around croplands like vineyards with the aim and possibility of improving and/or sustaining biological pest management has been around for 10-20 years. Grapegrowers in the Walla Walla appellation experimented with this approach in the early 2000s but had no information on native plant species and their relative value to pest management and sustainability. Our project provides, for the first time, data on the effect and impact of restoring native plants and habitats on pest incidence, abundance and management. We show convincingly that beneficial insect and mite abundance is greater in vineyards that have enhanced native flora and habitats than in comparable nearby vineyards that do not encourage native plants and habitats.

For the first time we also have substantial information on the relative value of more than 100 flowering plant species (mostly native) in attracting beneficial insects. This will allow selection and use of endemic plants, adapted to the climate of eastern Washington and Oregon, in and around wine grape vineyards to improve the efficacy and sustainability of conservation biological control and integrated pest management. In addition, plants with benefits to pest management AND pollinator conservation may be selected.

Our research has uncovered a unique opportunity for grape growers to gain dual benefits from encouraging native flora and habitats. Aside from the clear economic benefit of increasing populations of predatory and parasitic insects to improve biological control of pests, the establishment of native plants also provides resources for threatened populations of pollinators like butterflies and native bees. Grape growers have the opportunity and potential to become one of the first, if not the first, agricultural enterprise in the United States to play a significant role in butterfly and bee conservation.

• Table 6
• Table 5
• Photo 5: Tall Buckwheat (Eriogonum elatum)
• Photo 6: Northern Buckwheat (Eriogonum compositum)
• Photo 8: Habitat-enhanced vineyard site in the Columbia Gorge
• Figure 3
• Figure 8
• Figure 10
• Figure 11
• Figure 14
• Table 9
• Table 10
• Table 11
• Figure 15
• Table 4
• Photo 11: Beneficial bug, Orius tristicolor (Minute Pirate Bug)
• Photo 2: Sagebrush (Artemisia tridentata)
• Photo 3: Oregon Sunshine (Eriophylum lanatum)
• Photo 4: Yarrow (Achillea millefolium)
• Photo 7: Snow Buckwheat (Eriogonum niveum)
• Photo 9: Conventional vineyard site in the Columbia Gorge
• Figure 6
• Figure 7
• Photo 15: Boisduval’s blues are a candidate for restoration in vineyards
• Figure 1
• Figure 2
• Figure 12
• Photo 10: Beneficial beetle: Mite-eating ladybeetle, Stethorus punctum
• Photo 12: Parasitic wasp (Braconidae)
• Table 8
• Table 3
• Figure 9
• Figure 13
• Table 2
• Figure 4
• Figure 5
• Table 7
• Photo 13: Sheridan’s Hairstreak, a butterfly dependent on Buckwheat (Eriogonum spp.)