A roadmap for ladybird conservation and recovery.

Ladybirds (Coleoptera: Coccinellidae) provide services that are critical to food production, and they fulfill an ecological role as a food source for predators. The richness, abundance, and distribution of ladybirds, however, are compromised by many anthropogenic threats. Meanwhile, a lack of knowledge of the conservation status of most species and the factors driving their population dynamics hinders the development and implementation of conservation strategies for ladybirds. We conducted a review of the literature on the ecology, diversity, and conservation of ladybirds to identify their key ecological threats. Ladybird populations are most affected by climate factors, landscape composition, and biological invasions. We suggest mitigating actions for ladybird conservation and recovery. Short-term actions include citizen science programs and education, protective measures for habitat recovery and threatened species, prevention of the introduction of non-native species, and the maintenance and restoration of natural areas and landscape heterogeneity. Mid-term actions involve the analysis of data from monitoring programs and insect collections to disentangle the effect of different threats to ladybird populations, understand habitat use by taxa on which there is limited knowledge, and quantify temporal trends of abundance, diversity, and biomass along a management-intensity gradient. Long-term actions include the development of a worldwide monitoring program based on standardized sampling to fill data gaps, increase explanatory power, streamline analyses, and facilitate global collaborations.

Las catarinas (Coleoptera: Coccinellidae) proporcionan servicios que son críticos para la producción de alimento, y juegan un papel ecológico como fuente de alimento para depredadores. Sin embargo, la riqueza, abundancia y distribución de catarinas están en peligro debido a muchas amenazas antropogénicas. La carencia de conocimiento sobre el estatus de conservación de la mayoría de las especies y los factores que inciden en su dinámica poblacional dificulta el desarrollo e implementación de estrategias de conservación para las catarinas. Realizamos una revisión de la literatura sobre la ecología, diversidad y conservación de catarinas para identificar sus amenazas ecológicas clave. Las poblaciones de catarinas fueron afectadas mayormente por factores climáticos, composición del paisaje e invasiones biológicas. Proponemos acciones de mitigación para la conservación y recuperación de catarinas. Acciones a corto plazo incluyen programas de ciencia y educación ciudadana, medidas de protección para la recuperación de hábitat y de especies amenazadas, prevención de la introducción de especies no nativas y el mantenimiento y restauración de áreas naturales y la heterogeneidad del paisaje. Acciones a mediano plazo implican el análisis de datos obtenidos de programas de monitoreo y colecciones de insectos para desenmarañar el efecto de las diferentes amenazas a las poblaciones de catarinas, comprender el uso del hábitat por taxa de los que se tiene conocimiento limitado y cuantifica las tendencias temporales de la abundancia, diversidad y biomasa a lo largo de un gradiente de intensidad de manejo. Acciones a largo plazo incluyen el desarrollo de un programa de monitoreo a nivel mundial basado en muestreos estandarizados para subsanar la falta de datos, incrementar el poder explicativo, optimizar los análisis y facilitar colaboraciones globales.

Virulence of the insect-pathogenic fungi Metarhizium spp. to Mormon crickets, Anabrus simplex (Orthoptera: Tettigoniidae).

The Mormon cricket (MC), Anabrus simplex Haldeman, 1852 (Orthoptera: Tettigoniidae), has a long and negative history with agriculture in Utah and other western states of the USA. Most A. simplex populations migrate in large groups, and their feeding can cause significant damage to forage plants and cultivated crops. Chemical pesticides are often applied, but some settings (e.g. habitats of threatened and endangered species) call for non-chemical control measures. Studies in Africa, South America, and Australia have assessed certain isolates of Metarhizium acridum as very promising pathogens for Orthoptera: Acrididae (locust) biocontrol. In the current study, two isolates of Metarhizium robertsii, one isolate of Metarhizium brunneum, one isolate of Metarhizium guizhouense, and three isolates of M. acridum were tested for infectivity to MC nymphs and adults of either sex. Based on the speed of mortality, M. robertsii (ARSEF 23 and ARSEF 2575) and M. brunneum (ARSEF 7711) were the most virulent to instars 2 to 5 MC nymphs. M. guizhouense (ARSEF 7847) from Arizona was intermediate and the M. acridum isolates (ARSEF 324, 3341, and 3609) were the slowest killers. ARSEF 2575 was also the most virulent to instar 6 and 7 nymphs and adults of MC. All of the isolates at the conidial concentration of 1 × 107 conidia ml-1 induced approximately 100% mortality by 6 days post application of fungal conidia. In conclusion, isolates ARSEF 23, ARSEF 2575, and ARSEF 7711 acted most rapidly to kill MC under laboratory conditions. The M. acridum isolates, however, have much higher tolerance to heat and UV-B radiation, which may be critical to their successful use in field application.

Summer Development and Survivorship of the Weed Biocontrol Agent, Mecinus janthiniformis (Coleoptera: Curculionidae), Within Stems of Its Host, Dalmatian Toadflax (Lamiales: Plantaginaceae), in Utah.

The summer phenology and survivorship of the stem-mining weevil, Mecinus janthiniformis Tosevski and Caldara, a biocontrol agent of Dalmatian toadflax, Linaria dalmatica (L.) Miller, was studied in 2015-2016 as it developed within host plant stems at a low elevation, open rangeland site in northern Utah. Hatching from eggs in spring and early summer, weevils occurred as larvae within stems in June. Earliest maturing adults occurred in mid-July, and the majority of individuals had completed pupal development by early August. Survivorship within stems was high, with two-thirds or more of individuals surviving from egg hatch to adulthood as assessed in mid-September. Mortality rates within stems were highest during larval development, with parasitism accounting for the majority of deaths. At least three parasitoid species (Chalcidoidea: Pteromalidae and Eupelmidae), including both endoparasitoids and ectoparasitoids, were found attacking weevils within stems. Although most surviving weevils remained as adults within stems to overwinter, some adults were found to have chewed exit holes, and in some cases had exited from stems, beginning in July; the fate of these prematurely exiting adults is unknown. Low summer mortality rates within stems should promote weevil establishment under the hot, dry conditions of northern Utah, but parasitism and premature exiting of adults from host stems merit further investigation concerning their potential to reduce biocontrol efficacy. The results presented here for M. janthiniformis phenology within host stems will contribute to the development of standardized, summer monitoring for this biocontrol agent by stem dissection.

Dispersal in Host⁻Parasitoid Interactions: Crop Colonization by Pests and Specialist Enemies.

Interactions of insect pests and their natural enemies increasingly are being considered from a metapopulation perspective, with focus on movements of individuals among habitat patches (e.g., individual crop fields). Biological control may be undercut in short-lived crops as natural enemies lag behind the pests in colonizing newly created habitat. This hypothesis was tested by assessing parasitism of cereal leaf beetle (Oulema melanopus) and alfalfa weevil (Hypera postica) larvae at varying distances along transects into newly planted fields of small grains and alfalfa in northern Utah. The rate of parasitism of cereal leaf beetles and alfalfa weevils by their host-specific parasitoids (Tetrastichus julis (Eulophidae) and Bathyplectes curculionis (Ichneumonidae), respectively) was determined for earliest maturing first generation host larvae. Rates of parasitism did not vary significantly with increasing distance into a newly planted field (up to 250⁻700 m in individual experiments) from the nearest source field from which pest and parasitoid adults may have immigrated. These results indicate strong, rapid dispersal of the parasitoids in pursuing their prey into new habitat. Thus, across the fragmented agricultural landscape of northern Utah, neither the cereal leaf beetle nor the alfalfa weevil initially gained substantial spatial refuge from parasitism by more strongly dispersing than their natural enemies into newly created habitat. Additional studies, including those of colonization of newly planted crops by generalist pests and natural enemies, are called for in assessing these results with a broader perspective.

Phenology of the Dalmatian Toadflax Biological Control Agent Mecinus janthiniformis (Coleoptera: Curculionidae) in Utah.

The phenology of the stem-mining weevil Mecinus janthiniformis Tosevski and Caldara (Coleoptera: Curculionidae) as adults attacking Dalmatian toadflax, Linaria dalmatica (L.) Miller (Plantaginaceae), was studied in 2014-2015 at two low elevation sites in northern Utah. The seasonal pattern of adult weevil abundance on the host plant at the two sites was most similar between years when described by degree-day accumulation, versus calendar date. Repeated censusing over the growing season revealed that males appeared first and subsequently peaked in abundance on the host plant earlier than females did, such that the adult population was dominated by males early in the season and by females late in the season. Peak female abundance on the host plant occurred at the time when Dalmatian toadflax stems reached their maximum height and density and when they began flowering widely. Maximum toadflax stem heights and densities, and flowering activity, were markedly reduced in 2015 compared to 2014. In contrast to these host plant parameters that vary between years, degree-day accumulation can be used readily for timing collection and survey efforts for adult weevils and female adult weevils in particular. Use of degree-day accumulation can thereby facilitate implementation of redistribution and monitoring programs for M. janthiniformis as a biological control agent of Dalmatian toadflax.

Estimating Prey Consumption in Natural Populations of Harmonia axyridis (Coleoptera: Coccinellidae) Using Production of Feces.

Production of feces (PF) is a useful proxy indicating quantity of ingested food. Although influenced by many uncontrolled factors PF provides insight into food consumption under natural conditions. In Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) variation in PF was investigated in populations of various hostplants at localities of central Bohemia (50N, 14E), throughout the season of 2016. The adults collected from these hostplants were starved for 48 h at standard conditions, and dry mass of feces produced during this period was measured. Despite enormous differences in PF among individuals, significant variation over the season occurred in average PF of both males and females. PF increased with abundance of aphids and was significantly greater in females than males. Gravidity, as manifested through oviposition within 48 h after capture, was associated with increased PF, while hostplant and color morph did not affect variation in PF among individuals. From PF as measured in this study, it can be estimated that at sites hosting abundant aphid populations H. axyridis (as an adult male or female) may consume 19 (male) to 45 (female) aphids per day (assumed body length 1mm). In the absence of aphids, adults may consume one to nine individuals of alternative prey per day (body length 1-2 mm).

Biodiversity, ecosystem functioning, and classical biological control.

Increasing concern over worldwide loss of biodiversity has led ecologists to focus intently on how ecosystem functioning may depend on diversity. In applied entomology, there is longstanding interest in the issue, especially as regards the importance of natural enemy diversity for pest control. Here I review parallels in interest, conceptual framework, and conclusions concerning biodiversity as it affects ecosystem functioning in general and classical biological control in particular. Whereas the former focuses on implications of loss of diversity, the latter focuses on implications of increase in diversity as additional species of natural enemies are introduced to novel communities in new geographic regions for insect pest and weed control. Many field studies now demonstrate that ecosystem functioning, e.g., as reflected in primary productivity, is enhanced and stabilized over time by high diversity as the community increases in its efficiency in exploiting available resources. Similarly, there is growing field support for the generalization that increasing species and functional diversity of natural enemies leads to increasing pest suppression. Nonetheless a central concern of classical biological control in particular, as it seeks to minimize non-target effects, remains as to whether one or a few species of natural enemies can provide sufficient pest control.

Do defensive chemicals facilitate intraguild predation and influence invasion success in ladybird beetles?

Egg predation and cannibalism are believed to be common phenomena among many species of aphidophagous predatory ladybird beetles despite the presence of alkaloid based defensive chemicals in all life stages. We identified defensive chemicals from eggs of three congeneric species, one introduced into North America (Coccinella septempunctata L.), and two native (C. transversoguttata richardsoni Brown, and C. novemnotata Herbst), and examined the effects of ingested defensive chemicals on first instars. Ingested congeneric alkaloids were not toxic to first instars, likely because the three congeners produce the same principal alkaloids, precoccinelline and coccinelline, in similar amounts. First instars of the three congeners accumulated alkaloids ingested through egg cannibalism and congeneric predation. Egg consumption doubled the amount of alkaloids in first instars when they fed on conspecific or congeneric eggs, in comparison to a pea aphid diet. No detrimental effects of ingested congeneric alkaloids on development or survival of first instars were observed among these congeners. Chemical defenses of eggs are therefore not likely to be important in favoring the invasive species, C. septempunctata, in interactions with these native congeneric species. Because the invasive species is the most aggressive predator, having the same types of alkaloids may facilitate disproportionate intraguild predation on native congeners by C. septempunctata thereby potentially enhancing the invasion success of this introduced species.

Spatial and temporal dynamics of Aroga moth (Lepidoptera: Gelechiidae) populations and damage to sagebrush in shrub steppe across varying elevation.

Spatial and temporal variation in the density of the Aroga moth, Aroga websteri Clarke (Lepidoptera: Gelechiidae), and in its damage to its host plant, big sagebrush (Artemisia tridentata Nuttall), were examined at 38 sites across a shrub steppe landscape in mountain foothills of northern Utah. Sites were sampled from 2008 to 2012 during and after an outbreak of the moth, to assess whether and how local variation in moth abundance, survivorship, and damage to the host plant was accounted for by sagebrush cover, elevation, slope, aspect, or incident solar radiation. As moth numbers declined from a peak in 2009, individual sites had a consistent tendency in subsequent years to support more or fewer defoliator larvae. Local moth abundance was not correlated with sagebrush cover, which declined with elevation, and moth survivorship was highest at intermediate elevations (1,800-2,000 m). North-facing stands of sagebrush, characterized by lower values of incident solar radiation, were found to be especially suitable local habitats for the Aroga moth, as reflected in measures of both abundance and feeding damage. This high habitat suitability may result from favorable microclimate, both in its direct effects on the Aroga moth and in indirect effects through associated vegetative responses. North-facing sites also supported taller and more voluminous sagebrush plants in comparison to south-facing sites. Thus, the moth is reasonably predictable in the sites at which it is likely to occur in greatest numbers, and such sites may be those that in fact have most potential to recover from feeding damage.

Infestation of grain fields and degree-day phenology of the cereal leaf beetle (Coleoptera: Chrysomelidae) in Utah: long-term patterns.

Scouting at key times in the seasonal development of insect pest populations, as guided by degree-day accumulation, is important for minimizing unwarranted insecticide application. Fields of small grains in northern Utah were censused weekly from 2001 to 2011, to assess infestation by the cereal leaf beetle, Oulema melanopus (L.) (Coleoptera: Chrysomelidae), and develop degree-day guidelines for measuring cereal leaf beetle abundance at peak egg and larval densities in any given year. Even in years of high overall numbers of cereal leaf beetle, relatively few fields were heavily infested (with 20 or more cereal leaf beetle eggs + larvae per 0.09 m2) at either egg or larval peak density during the growing season. In individual fields, the number of immature cereal leaf beetle (eggs + larvae) at peak larval density was positively related to the number of immature cereal leaf beetles present earlier at peak egg density. Although there was large variation among years in when cereal leaf beetle egg and larval numbers peaked during the season as measured by degree-day accumulation from 1 January, much of this variation was accounted for by the warmth of the early spring before significant egg laying occurred. Hence, degree-day estimates that account for early spring warmth can guide growers in scouting grain fields at peak egg densities to identify fields at high risk of subsequent economic damage from cereal leaf beetle larval feeding. The relatively low incidence of fields heavily infested by cereal leaf beetle in northern Utah emphasizes the benefit that growers can gain by scouting early before applying insecticide treatments.

Frass analysis of diets of aphidophagous lady beetles (Coleoptera: Coccinellidae) in Utah alfalfa fields.

Aphidophagous lady beetles enhance their foraging success in natural settings by consuming other types of food in addition to aphids. Frass analysis was used to examine natural diets of female lady beetles in fields of alfalfa (Medicago sativa L.) in northern Utah. The first (spring) alfalfa crop was censused in 2004 and 2005 to determine the diet of female adults of the introduced Coccinella septempunctata L., and two native species, C. transversoguttata richardsoni Brown, and Hippodamia convergens Guerin. The proportion of females of the three lady beetle species that fed on pea aphids [Acyrthosiphon pisum (Harris)] and alfalfa weevil larvae [Hypera postica (Gyllenhal), an abundant alternative prey] increased from early to late season during the first crop. A corresponding seasonal decrease occurred in the proportion of females consuming other types of arthropods (e.g., thrips and collembolans) and nonarthropod food (pollen and fungal spores). Overall, frass analysis indicated that the diets of C. septempunctata and the two native species in alfalfa were similar in their inclusion of a broad variety of foods. The study shows that frass analysis can provide a good overview of the diets of lady beetles in natural settings.

Interactions over time between cereal leaf beetle (Coleoptera: Chrysomelidae) and larval parasitoid Tetrastichus julis (Hymenoptera: Eulophidae) in Utah.

The phenology of parasitism of the cereal leaf beetle, Oulema melanopus (L.) (Coleoptera: Chrysomelidae) by Tetrastichus julis (Walker) (Hymenoptera: Eulophidae) was studied in small grain fields from 2000 to 2005 in northern Utah, after release and redistribution of the partially bivoltine larval parasitoid during the 1990s. Host larvae first occurred in May, with peak infestation typically occurring in early to mid-June. Parasitism by overwintering females of T. julis was highest among earliest developing beetle larvae. Thereafter, rates of parasitism fell to low levels (5-10% or less) by the latter half of June, when heat accumulation had reached 280-350 degree-days (based on a minimum threshold of 8.9 degrees C). With the emergence of second generation parasitoids, rates of parasitism rose to levels approaching 100% among the relatively few late-developing larvae of O. inelanopus. Clear and consistent differences over the years were not observed among different crops of small grains (barley, wheat, or oats) either in the phenology and intensity of beetle infestation, or in the rate of parasitism of beetle larvae. The rate of parasitism was especially high in 2005, and an increase in the minimum level of parasitism (observed each year at mid-season) was apparent over the course of the study. These results indicate that the parasitoid has become well established and seems to be continuing to increase in its impact on O. melanopus in northern Utah, despite a relatively hostile environment of crop management, wherein most fields are plowed and disked annually.

Asymmetric larval interactions between introduced and indigenous ladybirds in North America.

Understanding the mechanisms that result in the success of introduced species will contribute to predicting future invasions and managing invaded systems. We examined interactions between larvae of two predatory ladybird species recently introduced to North America, Coccinella septempunctata (CS) and Harmonia axyridis (HA), and two indigenous ladybirds, Coccinella transversoguttata (CT) and Hippodamia convergens (HC). By pairing young and old larvae in the laboratory at low and high levels of aphid availability, we assessed the degree of asymmetry in intraguild predation (IGP), the strength of competitive effects on growth and development of larvae escaping predation, and the nature of attack and escape behavior among the species. Interactions were generally asymmetric, with larvae of introduced species acting most frequently as intraguild predators and larvae of indigenous species serving most frequently as intraguild prey (the two Coccinella spp., however, preyed on each other at similar rates). Because they were especially aggressive and because other larvae were least successful in escaping their attacks, larvae of HA had stronger negative effects on larvae of the two indigenous species than did larvae of CS. Such negative effects, expressed most strongly when aphid availability was low, were especially adverse for the smaller of the two indigenous species, HC. In general, older larvae interacted with each other more strongly than young larvae did, and older larvae had especially strong negative effects on young larvae when interactions occurred between age classes. Our results suggest that HA more than CS may represent a threat to indigenous ladybirds as an intraguild predator, and that IGP in turn may play a stronger role for HA than for C. septempunctata in promoting the successful invasion of North America.

Essential versus alternative foods of insect predators: benefits of a mixed diet.

Although many predatory insects appear to be opportunistic generalists in their selection of prey, only a subset of prey species may in fact serve as "essential foods" capable of supporting immature growth and adult reproduction. It has been suggested that other, "alternative foods" serve only to maintain the predator when essential foods are not available, but little research has evaluated the significance of a mixed diet of essential and alternative foods for predator growth or reproduction. Here we test the general hypothesis that although alternative prey may be inadequate to support reproduction when consumed alone by adult predators, consumption of such prey may enhance the predator's reproductive output when the predator also has access to essential prey. We compared egg production by two aphidophagous lady beetles, Coccinella septempunctata and C. transversoguttata, provided with diets of aphids (essential prey) and weevils (alternative prey). As predicted, female predators produced greater numbers of eggs when a diet of pea aphids in limited number was supplemented by alfalfa weevil larvae. The predators laid no eggs when provided only with weevils or only with sugar. But once aphids were added to the diet, females of C. transversoguttata (but not C. septempunctata) laid eggs in greater numbers when they had fed previously on weevils than on sugar. Females of both species also produced eggs in modest numbers when provided with both weevils in excess and sugar, but this diet supported a lower rate of egg production than did a diet of weevils in excess plus a limited number of aphids. Although C. septempunctata has a longer history of association with the alfalfa weevil than does C. transversoguttata, the former species was not more effective in exploiting this alternative prey in support of reproduction. The tendency of generalist predators such as adult lady beetles to consume alternative as well as essential prey probably enhances considerably their ability to capitalize on short-lived and scattered opportunities as they seek out suitable sites in which to reproduce.

Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids.

The nature and relative strengths of intra versus interspecific interactions among foraging ladybeetle larvae were studied experimentally by measuring short-term growth rates of predators and reductions in population sizes of prey in laboratory microcosms. In these microcosms, ladybeetle larvae foraged singly or as conspecific or heterospecific pairs, for pea aphids on bean plants over a two-day period. Similarly sized third instar larvae ofHippodamia convergens andH. tredecimpunctata, H. convergens andH. sinuata, andH. convergens andCoccinella septempunctata, were tested in experiments designed to ensure that paired larvae experienced moderate competition. Interspecific competition in these experiments did not differ significantly from intraspecific competition, in that an individual's weight gain did not depend on whether its competitor was heterospecific or conspecific. Furthermore, aphid populations were reduced equally by heterospecific and conspecific pairs. These results suggest that there is little or no difference between intra and interspecific interactions among larvae of these ladybeetles when two similarly sized individuals co-occur on a host plant. Thus, the species diversityper se of assemblages of ladybeetle larvae may have little influence over the short term on the reduction of aphid populations by ladybeetle predation.

Timing of reproduction in a prairie legume: seasonal impacts of insects consuming flowers and seeds.

Seasonal patterns of insect damage to reproductive tissue of the legume Baptisia australis were studied for three years in native tallgrass priairie. Contrasting seasonal patterns of damage were associated with the major species of insect consumers. The moth Grapholitha tristegana (Olethreutidae) and the weevil Tychius sordidus (Curculionidae), which together infested 80-100% of developing fruits (pods), consistently damaged more seeds on average in early than in late maturing pods. But while late opening flowers were less subject to attack from moths and weevils, they were more subject to attack from chewing insects, particularly blister beetles (Epicauta fabricii, Meloidae), which destroyed >80% of all flowers and developing young pods (including moth and weevil larval inhabitants). The blister beetles arrived late in the flowering season and fed particularly on young reproductive tissue, allowing larger, older pods that had developed from early opening flowers to escape destruction. The relative abundances and impacts of blister beetles, moths, and weevils varied from year to year. Adding to the uncertainty of reproductive success of the host plant were the large and variable amounts of damage to immature buds inflicted by insects (including the blister beetles and weevil adults) and late killing frosts. Thus, timing of flowering is critical to success in seed production for B. australis. The heavy impacts of insects and weather can result in a very narrow window in time (which shifts from year to year) during which B. australis can flower with any success. The opposing pressures exerted by insects and weather on floral reproductive success may act in concert with other features of the plant's biology to foster the maintenance of considerable diversity in flowering times among individuals in local populations of B. australis.