Insect ecology: Tracking migratory butterflies through pollen.

Painted ladies are well-known migratory butterflies, but confirmation of the details of their swarming flights through Europe has evaded scientists until now. It was their role as pollinators, carrying pollen grains on their flights, that helped unlock the secrets of their migrations.

Monarch Butterflies in Western North America: A Holistic Review of Population Trends, Ecology, Stressors, Resilience and Adaptation.

Monarch butterfly populations in western North America suffered a substantial decline, from millions of butterflies overwintering in California in the 1980s to less than 400,000 at the beginning of the 21st century. The introduction of neonicotinoid insecticides in the mid-1990s and their subsequent widespread use appears to be the most likely major factor behind this sudden decline. Habitat loss and unfavorable climates (high temperatures, aridity, and winter storms) have also played important and ongoing roles. These factors kept overwintering populations stable but below 300,000 during 2001-2017. Late winter storm mortality and consequent poor spring reproduction drove winter populations to less than 30,000 butterflies during 2018-2019. Record high temperatures in California during the fall of 2020 appeared to prematurely terminate monarch migration, resulting in the lowest overwintering population (1899) ever recorded. Many migrants formed winter-breeding populations in urban areas. Normal seasonal temperatures in the autumns of 2021 and 2022 enabled overwintering populations to return to around the 300,000 level, characteristic of the previous two decades. Natural enemies (predators, parasitoids, parasites, and pathogens) may be important regional or local drivers at times but they are a consistent and fundamental part of monarch ecology. Human interference (capture, rearing) likely has the least impact on monarch populations. The rearing of monarch caterpillars, particularly by children, is an important human link to nature that has positive ramifications for insect conservation beyond monarch butterflies and should be encouraged.

Reply to Davis, A.K. Monarchs Reared in Winter in California Are Not Large Enough to Be Migrants. Comment on "James et al. First Population Study on Winter Breeding Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) in the Urban South Bay of San Francisco, California. Insects 2021, 12, 946".

This is a reply to the comment from Davis [...].

First Population Study on Winter Breeding Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) in the Urban South Bay of San Francisco, California.

The western North American monarch butterfly population assessed by counts of non-reproductive overwintering butterflies at coastal sites in California declined to less than 2000 in 2020/21. Simultaneously, reports of reproductive monarchs increased in San Francisco urban areas, perhaps representing a shift in overwintering strategy. To better understand monarch winter breeding in the Bay area, we studied adult and immature populations in Santa Clara County during January-June 2021. Adult monarchs were common with numbers ranging from 0.23-1.54/min during ~30 min weekly surveys at one site, with lowest numbers late April to mid-May. Eggs and larvae, primarily on ornamental milkweeds, were found on nearly all survey dates with lowest numbers mid-late April to mid-May. Levels of infection of adults by the parasite Ophryocystis elektroscirrha were consistently high during the study (69.3-77.5%). From 499 monarchs tagged post-eclosion, recovery rates of 19.2-23.6% occurred from releases in January-February and May-June but only 11.9-13.0% from March-April releases. Although distances were small, butterflies tagged in April were recovered from greater distances than other months. Tagged monarchs flew primarily north or east. There were reduced numbers of adult monarchs during late April-mid-May with some evidence of northerly and easterly emigration at the same time from tagged butterflies, suggesting some movement out of the South Bay area, perhaps representing spring migration. We conclude that monarchs can successfully breed and maintain populations on ornamental milkweeds during winter at urban sites in the South Bay of San Francisco and may still migrate during spring to remain part of the wider western population.

Further Insights on the Migration Biology of Monarch Butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) from the Pacific Northwest.

The fall migration of monarch butterflies, Danaus plexippus (L.), in the Pacific Northwest was studied during 2017-2019 by tagging 14,040 captive-reared and 450 wild monarchs. One hundred and twenty-two captive-reared monarchs (0.87%) were recovered at distances averaging 899.9 ± 98.6 km for Washington-released and 630.5 ± 19.9 km for Oregon-released monarchs. The greatest straight-line release to recovery distance was 1392.1 km. A mean travel rate of 20.7 ± 2.2 km/day and maximum travel of 46.1 km/day were recorded. Recovery rates were greater for Oregon-released monarchs (0.92%) than Washington-released (0.34%) or Idaho-released monarchs (0.30%). Most monarchs (106/122) were recovered SSW-S-SSE in California, with 82 at 18 coastal overwintering sites. Two migrants from Oregon were recovered just weeks after release ovipositing in Santa Barbara and Palo Alto, CA. Two migrants released in central Washington recovered up to 360.0 km to the SE, and recoveries from Idaho releases to the S and SE suggests that some Pacific Northwest migrants fly to an alternative overwintering destination. Monarchs released in southern Oregon into smoky, poor quality air appeared to be as successful at reaching overwintering sites and apparently lived just as long as monarchs released into non-smoky, good quality air. Migration and lifespan for monarchs infected with the protozoan parasite, Ophryocystis elektroscirrha (McLaughlin and Myers), appeared to be similar to the migration and survival of uninfected monarchs, although data are limited. Our data improve our understanding of western monarch migration, serving as a basis for further studies and providing information for conservation planning.

A Neonicotinoid Insecticide at a Rate Found in Nectar Reduces Longevity but Not Oogenesis in Monarch Butterflies, Danaus plexippus (L.). (Lepidoptera: Nymphalidae).

The monarch butterfly in North America has suffered a serious population decline since the mid-1990s. The introduction and widespread use of neonicotinoid insecticides during the same time period has been suggested as a potential driver of this decline but no studies have looked at the impact of these insecticides on adult monarchs. A brief laboratory study assessed the impact of Imidacloprid, the most commonly used neonicotinoid, on western monarch butterfly longevity and oogenesis. Imidacloprid at 23.5 ppb, a field-realistic rate reported from wild nectar and pollen, was fed ad libitum to newly-eclosed monarchs in a sugar-based diet for 22 days. Treated monarchs showed reduced longevity, suffering 78.8% mortality by day 22, compared to 20% in untreated monarchs. Prior to death, butterflies exhibited signs of poisoning including uncoordinated flapping of wings and uncontrolled vibrating of wings and body. Imidacloprid did not reduce egg production. Shortened adult longevity has serious consequences for monarch population development, migration and overwintering. The potential widespread impact of imidacloprid-contaminated crop and wild flower nectar, may be a significant driver of monarch population decline. More research on the impact of neonicotinoid insecticides on the monarch and other butterflies should be viewed as a serious priority.

Identity and Seasonal Abundance of Beneficial Arthropods Associated with Big Sagebrush (Artemisia tridentata) in Central Washington State, USA.

Big sagebrush (Artemisia tridentata) characterizes and dominates the sagebrush steppe, the largest temperate semi-desert ecosystem in North America. The beneficial arthropod fauna hosted by A. tridentata is poorly known but could be of importance to nearby agriculture seeking to exploit biologically-based pest management. Over four years, we identified and assessed the seasonal abundance of beneficial arthropods (predators, parasitoids, pollinators) associated with A. tridentata during spring to autumn in the Yakima Valley of central Washington using sticky traps. During 2011⁻2014, 207 sticky traps were placed on non-blooming and blooming A. tridentata plants for a total of 966 trapping days. Overall, across all seasons, we trapped 259.7 beneficial arthropods per trap and 92% of these were parasitoid wasps. Significantly greater numbers of beneficial arthropods were associated with blooming A. tridentata during autumn (410/trap) than non-blooming plants in the spring (181.3/trap) or summer (85.1/trap). Parasitoid wasps and predatory true bugs were most abundant during the autumn, but ladybeetles, lacewings, spiders, bees, and predatory thrips were most common during spring. The association of high numbers of predators, parasitoids, and pollinators with A. tridentata during blooming and non-blooming periods indicates that this plant is an important reservoir of beneficial arthropods in the sagebrush steppe of central Washington. Consequently, biologically-based pest management programs in central Washington may benefit from careful management and retention of A. tridentata plants on crop borders.

Beneficial Insect Attraction to Milkweeds (Asclepias speciosa, Asclepias fascicularis) in Washington State, USA.

Native plant and beneficial insect associations are relatively unstudied yet are important in native habitat restoration programs for improving and sustaining conservation biological control of arthropod pests in agricultural crops. Milkweeds (Asclepias spp.) are currently the focus of restoration programs in the USA aimed at reversing a decline in populations of the milkweed-dependent monarch butterfly (Danaus plexippus); however, little is known of the benefits of these plants to other beneficial insects. Beneficial insects (predators, parasitoids, pollinators) attracted to two milkweed species (Asclepias speciosa, Asclepias fascicularis) in central Washington State, WA, USA were identified and counted on transparent sticky traps attached to blooms over five seasons. Combining all categories of beneficial insects, means of 128 and 126 insects per trap were recorded for A. speciosa and A. fascicularis, respectively. Predatory and parasitic flies dominated trap catches for A. speciosa while parasitic wasps were the most commonly trapped beneficial insects on A. fascicularis. Bees were trapped commonly on both species, especially A. speciosa with native bees trapped in significantly greater numbers than honey bees. Beneficial insect attraction to A. speciosa and A. fascicularis was substantial. Therefore, these plants are ideal candidates for habitat restoration, intended to enhance conservation biological control, and for pollinator conservation. In central Washington, milkweed restoration programs for enhancement of D. plexippus populations should also provide benefits for pest suppression and pollinator conservation.

Beneficial insects attracted to native flowering buckwheats (Eriogonum Michx) in central Washington.

Native plant and beneficial insect associations are relatively unstudied yet are important in native habitat restoration programs aimed at improving conservation biological control in perennial crops such as wine grapes. Beneficial insects (predators, parasitoids, pollinators) attracted to 10 species of flowering native wild buckwheat (Eriogonum spp.) in central Washington were identified and counted on transparent sticky traps. Combining all categories of beneficial insects, the mean number per trap ranged from 48.5 (Eriogonum umbellatum) to 167.7 (Eriogonum elatum). Three Eriogonum spp. (E. elatum, Eriogonum compositum, and Eriogonum niveum) attracted significantly more beneficial insects than the lowest-ranked species. E. niveum attracted greatest numbers of bees and parasitic wasps, and E. elatum was highly attractive to predatory true bugs and beneficial flies. Blooming periods of Eriogonum spp. extended from mid April to the end of September. This study demonstrates the attraction of beneficial insects to native flowering buckwheats and suggests their potential as a component of habitat restoration strategies to improve and sustain conservation biological control in Washington viticulture.

Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects.

Fifteen synthetic herbivore-induced plant volatiles (HIPVs) were field-tested for attractivity to beneficial insects in two experiments conducted in an open field and a hop yard in Washington State. Eleven insect species or families showed significant attraction to 13 HIPVs. The ladybeetle, Stethorus punctum picipes, was attracted to sticky traps baited with methyl salicylate (MeSA), cis-3-hexen-1-ol (He), and benzaldehyde (Be). The minute pirate bug, Orius tristicolor, was attracted to traps baited with MeSA, He, Be, and octyl aldehyde (Oa), and the bigeyed bug, Geocoris pallens, responded to MeSA, indole, and trans-2-hexen-1-al. The mymarid wasp, Anagrus daanei, was attracted to He, Oa, and farnesene. The chloropid fly, Thaumatomyia glabra, was highly attracted to methyl anthranilate. Insect families responding to HIPVs included Syrphidae (MeSA, He), Braconidae ((Z)-3-hexenyl acetate, He, cis-jasmone (J), methyl jasmonate (MeJA), methyl anthranilate (MeA)), Empididae (MeSA), Sarcophagidae (MeSA, Be, J, nonanal and geraniol), Tachinidae (Be), and Agromyzidae (MeSA). Micro-Hymenoptera (primarily parasitic wasp families) were attracted to MeSA, He, and indole. These results are discussed with respect to known properties and bioactivity of the tested HIPVs and to their potential as tools for recruiting natural enemies into agroecosystems.

Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops.

Evidence for recruitment and retention of beneficial insects in grapes and hops using controlled-release dispensers of methyl salicylate (MeSA), a component of herbivore-induced volatile blends, is presented. In a replicated experiment conducted in a juice grape vineyard, sticky cards in blocks baited with MeSA captured significantly greater numbers of five species of predatory insects (Chrysopa nigricornis, Hemerobius sp., Deraeocoris brevis, Stethorus punctum picipes, Orius tristicolor) than unbaited blocks. Four insect families (Syrphidae, Braconidae, Empididae, Sarcophagidae) were also significantly more abundant in the MeSA-baited blocks, as indicated by sticky card captures. Canopy shake samples and sticky card monitoring conducted in a MeSA-baited, unsprayed hop yard indicated development and maintenance of a beneficial arthropod population that was nearly four times greater than that present in an unbaited reference yard. Four times as many S. punctum picipes and six times as many O. tristicolor were sampled in the MeSA yard. Similar contrasts in abundance of these predators and others were apparent when compared with levels recorded in the yard in previous years. The large population of predatory insects in the MeSA-baited hop yard was associated with a dramatic reduction in spider mite numbers, the major arthropod pest of hops, in late June, and subeconomic populations were maintained for the rest of the season. The evidence presented here is highly suggestive that the use of controlled-release MeSA in a crop could increase recruitment and residency of populations of certain beneficial insects. This strategy may have the potential to enhance the efficacy and reliability of conservation biological control in crop pest management.

Effect of buprofezin on survival of immature stages of Harmonia axyridis, Stethorus punctum picipes (Coleoptera: Coccinellidae), Orius tristicolor (Hemiptera: Anthocoridae), and Geocoris spp. (Hemiptera: Geocoridae).

The effect of buprofezin, a chitin synthesis inhibitor, on development and survival of immature stages of Harmonia axyridis (Pallas), Stethortus punctum picipes Casey, Orius tristicolor (White), Geocoris pallens Stål, and Geocoris punctipes (Say), was examined in a series of laboratory bioassays. Very few H. axyridis larvae (3.1%) treated with buprofezin reached adulthood, although 65% of treated pupae emerged successfully. Buprofezin caused no mortality to eggs of S. punctum picipes but 71.1% of treated early instar larvae failed to complete development. Eighty percent of treated late instars and 92.3% of pupae produced viable adults. Early instar nymphs of O. tristicolor were unaffected by buprofezin, whereas 47.7 and 85% of G. punctipes and G. pallens nymphs, respectively, failed to complete development. Treated eggs of G. pallens hatched successfully. The use of buprofezin in integrated pest management in Washington state wine grapes is discussed.

Bioactivity, synthesis, and chirality of the sex pheromone of currant stem girdler, Janus integer.

It was previously reported that females of the currant stem girdler, Janus integer Norton (Hymenoptera: Cephidae), produce a compound, (Z)-9-octadecen-4-olide (1), that is sensitively detected by the antennae of males only. These characteristics suggested a pheromonal function, and this has now been confirmed with behavioral tests. Field tests conducted during two seasons in a commercial red currant field in Washington State showed that synthetic racemic 1 is attractive to male J. integer under natural conditions. A clear dose-response was evident, with greatest numbers of girdlers caught in sticky traps baited with 10 mg of the pheromone (in rubber septa) and least in traps baited with 1 mg or less. During May 2002, 10, 5, 3, and 1 mg baited traps caught means of 41.4, 26.6, 6.7, and 2.7 males/trap/visit (3-5 day intervals), respectively, with a maximum of 229 males caught in a single trap baited with 5 mg. A new synthetic method for racemic 1 is presented. The absolute configuration of natural 1 from the male sawflies was determined to be (R). The potential for using the sex pheromone of J. integer to improve management of this currant and gooseberry pest is discussed.

Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis.

Synthetic methyl salicylate (MeSA), a herbivore-induced plant volatile (HIPV), was demonstrated to be an attractant for the green lacewing, Chrysopa nigricornis, in two field experiments conducted in a Washington hop yard. Significantly greater numbers of C. nigricornis were trapped on MeSA-baited sticky cards (mean: 2.8 +/- 0.4/card/week) than on unbaited cards (0.45 +/- 0.15) during June-September. Cards baited with two other HIPVs, hexenyl acetate and dimethyl nonatriene, did not attract more C. nigricornis than did unbaited traps (0.30 +/- 0.10, 0.44 +/- 0.15, respectively). MeSA-baited Unitraps captured 1.9 +/- 0.5 C. nigricornis/trap/week during July-August compared to 0.20 +/- 0.20/trap/week in methyl eugenol-baited traps and 0.03 +/- 0.03/trap/week in unbaited traps. The potential use of MeSA in enhancing C. nigricornis populations in Washington hop yards as an aid to conservation biological control of aphids and mites is discussed.

Toxicity of imidacloprid to Galendromus occidentalis, Neoseiulus fallacis and Amblyseius andersoni (Acari: Phytoseiidae) from hops in Washington State, USA.

The toxicity of systemic and spray formulations of imidacloprid to Galendromus occidentalis Nesbitt, Neoseiulus fallacis Garman and Amblyseius andersoni (Chant) from hop yards in Washington State was evaluated in laboratory bioassays. The field rate of imidacloprid for hop aphids (0.13 g a.i. l) was highly toxic (100% mortality) to G. occidentalis and N. fallacis but less so (35.6% mortality) to A. andersoni. Half and quarter rates were also highly toxic to G. occidentalis and N. fallacis (79.5-100% mortality) but again had lower toxicity to A. andersoni (8.2-31.3% mortality). Systemic toxicity (via consumption of spider mite motiles feeding on leaf discs cut from imidacloprid-treated (0.13 g a.i. l) dwarf bean plants) was also high for G. occidentalis (98.3% mortality), as was toxicity from dried residues (93-98% mortality). Residual toxicity to N. fallacis was also high (89% mortality). The significance of these results for biological control of spider mites in hops and other crops is discussed.

Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid.

The effect of imidacloprid on fecundity in twospotted spider mites, Tetranychus urticae Koch, was investigated in laboratory experiments using individual females on bean leaf discs. Mites were directly exposed to spray formulations of imidacloprid or fed on discs cut from a systemically treated bean plant. Imidacloprid-treated T. urticae produced 10-26% more eggs during the first 12 d of adult life and 19-23% more during adulthood compared with a water-only treatment. Increased egg production occurred immediately after exposure and lasted for about 15 d in sprayed mites. In mites exposed to imidacloprid by ingestion, increased egg production was not apparent until after 6 d and lasted until about day 18. Longevity was significantly greater in mites that ingested imidacloprid but not in sprayed mites. The significance and importance of imidacloprid-stimulation of fecundity in T. urticae to pest management in crop systems like hops, which routinely use this insecticide, is discussed.