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Development of Behaviorally-Based Monitoring Tools for the Brown Marmorated Stink Bug (Heteroptera: Pentatomidae) in Commercial Tree Fruit Orchards
Abstract
Captures of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), were significantly greater in pyramid traps baited with the known attractant, methyl (2E,4E,6Z)decatrienoate, compared with unbaited traps. A dose-dependent response by adults to lures formulated with increasing amounts of methyl (2E,4E,62)-decatrienoate and deployed in association with black pyramid traps also was observed. Among pyramid traps representing different visual stimuli including black, green, yellow, clear, white and yellow, significantly greater captures were recorded in baited black pyramid traps for adults in 2009 and nymphs in 2010 compared with other trap types; the dark upright silhouette created by this trap likely represents a trunk-mimicking visual stimulus to foraging bugs. A ground-deployed baited black pyramid trap also captured significantly greater numbers of nymphs and adults compared with canopydeployed commercially available baited traps from Japan. Based on semi-field cage studies, brown marmorated stink bug was confirmed to be bivoltine within the mid-Atlantic region. Thus, the need for a reliable monitoring tool to detect presence, abundance and seasonal activity of brown marmorated stink bug in tree fruit and other cropping systems is critical.
... Despite consistent reports of increased H. halys pressure in orchard crop borders next to favorable habitats such as woodlots (Bergh et al. 2021), reports from the Mid-Atlantic region based on fruit injury suggested that H. halys pest pressure can vary considerably among locations within a relatively small geographic area (Joseph et al. 2014). Moreover, although many pheromone-based H. halys monitoring studies in the United States have been conducted in proximity to tree fruit orchards (Leskey et al. 2012c, Morrison et al. 2015, Acebes-Doria et al. 2020, Bergh et al. 2021), there has not been a systematic comparison of H. halys captures among sites near one another, including sites with and without the presence of a suitable cultivated crop serving as a feeding host. Quantifying differences in H. halys relative abundance among and between orchard and nonorchard sites and examining the biotic factors such as woody host plant species composition in adjoining woodlots may reveal new insights into factors underlying the site-specific differences in H. halys pressure reported. ...
The invasive Halyomorpha halys (Hemiptera: Pentatomidae) has threatened Mid-Atlantic tree fruit since 2010. To identify factors underlying observed differences in H. halys pest pressure among individual orchards within a geographically proximate area, a 3-yr study was conducted across 10 apple orchard and 8 nonorchard sites bordered by unmanaged woodlots. At each site, 3 pheromone traps were monitored weekly for H. halys captures from late April to mid-October. Apple injury was assessed at harvest at orchard sites annually, and a survey of woody plants found in woodlots adjacent to all sites was conducted. There were no significant differences in captures between orchard and nonorchard site types, but captures were significantly different among individual orchard sites and among individual nonorchard sites. A significant positive relationship between the amount of stink bug injury on apple at harvest and late season captures was detected at orchard sites in 2018 and 2019. Among woodlots adjacent to all sites, a significant positive relationship between the proportion of Lonicera spp. and mid- and late-season nymphal captures was identified. Season-long nymphal captures were positively related to the proportion of Lonicera and Elaeagnus and negatively with Sassafras. For adults, captures were negatively related to the proportion of Ailanthus and positively related to the proportion of Fraxinus in the early and mid-season, respectively. Our results indicate that orchard presence was not driving the relative abundance of localized H. halys populations and that differences in relative densities among sites point to other factors, such as abundance of specific uncultivated woody hosts in unmanaged areas.
... The benefits of pheromone-based monitoring include affordability, specificity to certain species, and user-friendliness. However, the success of the process also depends on crucial factors such as the rate of pheromone release, the trap's design, its color, and the strategic placement of the traps [42,48,[52][53][54][55][56][57][58][59]. In the population monitoring technique, to monitor Conotrachelus nenuphar (Coleoptera: Curculionidae) apple trees were baited with grandisonic acid (aggregation pheromone) and benzaldehyde (synthetic fruit volatile) to attract curculio adults. ...
The intensive use of insecticides can result in environmental pollution and adverse effects on human health due to the issue of insecticide residue in the environment. To mitigate this, various control techniques, including cultural, biological, and biotechnical methods, or their combinations, can be employed to manage invasive species. One such biotechnical method that has become popular is the use of pheromones. Pheromone techniques enable early pest detection, population monitoring, mass trapping or annihilation, and mating disruption. To maximize their effectiveness, it is important to determine the exact pheromone component, optimization rate, trap design, and saturation rate for each species. In conclusion, implementing these different pheromone-based strategies is essential for providing effective pest management strategies that take regional variations in pheromones into account.
... However, a number of field and laboratory studies reported that H. halys is generally attracted by light (Nielsen et al. 2013;Lee et al. 2013;Endo et al. 2014;Leskey et al. 2015;Cambridge et al. 2017;Rondoni et al. 2022), in certain cases, individuals were shown to be attracted by dark objects (Toyama et al. 2011;Leskey et al. 2012b). Our behavioural experiments showed that H. halys possesses positive phototaxis for all sensed wavelengths. ...
The brown marmorated stink bug (Halyomorpha halys) is an invasive pest insect species, which was recently introduced from Asia to America and then to Europe. Besides causing serious damage in agriculture, this species also represents a source of intense annoyance for humans in residential areas, because large amounts of individuals can aggregate on buildings while seeking shelter before overwintering. Taking into account the need for pesticide-free pest management methods, for example light trapping, we measured the spectral sensitivity of the compound eyes of H. halys with electroretinography (ERG). In behavioural experiments, we also quantified the attraction of H. halys to 14 quasi-monochromatic light stimuli in the 368–743 nm spectral range. The dark-adapted compound eyes were mostly sensitive to the green range, but a minor sensitivity peak in the UV region was also identified. Recordings on chromatic-adapted eye preparations unequivocally revealed the presence of only a green- and a UV-sensitive photoreceptor type, with sensitivity maxima at 519 nm and 367 nm, respectively. No sign of any blue-sensitive receptor was detected, and thus only a receptor set allowing dichromatic vision was found. Based on the results of the behavioural experiments, we established that the attraction of H. halys to light is increasing with decreasing wavelength, and thus we emphasize the importance of short wavelength lights (368–455 nm) when phototactic attraction of H. halys is the aim.
... Euschistus spp. with yellow traps have been observed in comparison to white and green pyramid traps [200]. For H. halys, adults and nymphs seem to be more attracted to black pyramid traps than to yellow, white, green, and clear ones [234], for both plastic and wood traps [205]. Similar results have been obtained with black traps for Bagrada hilaris (Burmeister) [235]. ...
Knowledge of the biology of a pest is essential for building sustainable management programmes. Pentatomidae have a hemimetabolous life cycle with egg, nymphal, and adult life stages, which differ in morphological, ecological, and behavioural traits. Some of these traits, such as mating behaviour, pheromones (alarm and aggregation pheromones) and the acquisition of gut symbionts can be targeted for pest management strategies. Here, we review the available literature on these life history traits of the Pentatomidae with potential for use in management programmes. Pheromone-mediated aggregation and the disruption of symbiont acquisition are two important targets for Pentatomidae control. Other traits such as the use of alarm pheromones for enhancing natural enemies and substrate-borne vibration for mating disruption deserve further consideration. Colour vision and flight ability are still poorly studied, despite their potential importance for stink bug management.
... Pheromones have abundant benefits in terms of pest control, e.g., cheap and easy to use, specific, and highly reactive [62,63]. Monitoring insect pests with pheromone traps the right timings for the application of insecticides [64,65]. Besides, these chemicals also prevent the rate of mating, thus decreasing insect progeny. ...
Biopesticides are organic, biologically occurring substances that are used to regulate pests naturally. They are derived from natural sources such as plants, animals, and microbes. These are produced by organisms to defend themselves against various dangers. Natural pesticides are biodegradable, target specific, and least toxic. This chapter discusses the mechanisms and modes of action of various biopesticides from different origins. The worth of biopesticides lags the market for commercial pesticides. The market value for biopesticides can be improved by understanding the main obstacles and limitations faced by them. This chapter highlights the challenges encountered while using biopesticides and offers solutions to overcome these difficulties. Additionally, the potential for the creation of novel biopesticides is also covered. This chapter confirms that natural products can be used in place of synthetic pesticides in safe ways.
The invasive Halyomorpha halys is a serious pest for several fruit trees, causing millions of dollars of crop damage every year across the world’s major fruit-growing regions. Once established in an orchard, H. halys quickly becomes the predominant stink bug species and is a major season-long pest. Annual increases in the population size of H. halys have resulted in increased pest pressure and a growing risk of severe crop damage. Reliable monitoring is indispensable for H. halys control and management, providing comprehensive information on the seasonality of pest population dynamics, abundance, and interaction with the environment, and is essential for the successful implementation of integrated pest management (IPM) strategies to prevent crop damage. Our study followed the seasonal population dynamics of H. halys in three apple orchards in the Goriška region of western Slovenia over the period 2019–2021. Pherocon® Dual Panel Adhesive Traps (Trece Inc.) and pyramidal Rescue® Stink Bug Traps, both baited with Trécé lures (two-component H. halys aggregation pheromone + pheromone synergist), were used to monitor H. halys adults and nymphs weekly from late March to the end of November. Captures taken with both types of trap clearly describe the seasonal dynamics of H. halys, with the first occurrence of overwintering adults in April and May, and with two peak occurrences in adults, in the middle of summer and in the beginning of autumn, corresponding to the appearance of two generations per year in the study area. The growing trap captures observed during the 3-year monitoring period suggest that H. halys was only recently introduced to the area and that natural enemies have not yet been fully recruited. Pyramid traps captured significantly more adults and nymphs than clear sticky traps and provided accurate monitoring of H. halys life stages throughout the season. Regardless of the lower trap catches of adults and juveniles, clear sticky traps clearly displayed H. halys seasonal dynamics pattern. Therefore, their use is recommended as an early detection tool in areas where pests are not yet present, or in areas with small H. halys populations. Halyomorpha halys adult trap captures were higher in Šempeter orchards, within areas of great landscape diversity and a large share of urban land. The seasonal dynamics of H. halys over the 3-year period were closely related to weather conditions, with temperature and relative humidity as the major factors affecting population growth.
Riptortus pedestris (Fabricius) and Halyomorpha halys (Stål) are the major pests that feed on soybean pods, seeds, and fruits. Higher populations and damage occur during the soybean maturity stages (podding to harvest). To compare the feeding behavior of R. pedestris and H. halys, we used the six most cultivated cultivars (Daepung-2ho, Daechan, Pungsannamul, Daewon, Seonpung, and Seoritae) in Korea using the electropenetrography (EPG) technique. Both R. pedestris and H. halys, the NP (non-penetration), a non-probing waveform, was the shortest in the Pungsannamul (298 and 268 min) and the longest in the Daepung-2ho (334 and 339 min), respectively. The feeding waveforms Pb (phloem feeding: E1-Salivation and E2-Sap feeding) and G (xylem feeding) were the longest in Pungsannamul and the shortest in Daepung-2ho. In addition, as a result of investigating the damage rate by planting six cultivars of beans in the field, as expected, the proportions of damage types B and C were highest in Pungsannamul and lowest in Daepung-2ho. These results reveal that both bug species ingest xylem sap from leaflets and stems using a salivary sheath strategy to acquire water and nutrients from soybean pods/seeds with cell-rupture tactics. This study provides perceptive information to understand the feeding behavior, field occurrence, and damage patterns of R. pedestris and H. halys, which may have key implications for the management of hemipteran pests by determining the specificity and susceptibility of host plants.
Stink bugs comprise a significant and costly pest complex for numerous crops in the US, including row crops, vegetables, and tree fruits and nuts. Most management relies on the use of broad-spectrum and disruptive insecticides with high human and environmental risks associated with them. Growing concerns about pesticide resistance in stink bugs are forcing pest managers to explore safer and more sustainable options. Here, we review the diverse suite of natural enemies of stink bugs in the US, noting that the egg and the late nymphal and adult stages of stink bugs are the most commonly attacked by parasitoids, whereas eggs and young nymphs are the stages most commonly attacked by predators. The effectiveness of stink bugs’ natural enemies varies widely with stink bug species and habitats, influencing the biological control of stink bugs across crops. Historically, biological control of stink bugs has focused on introduction of exotic natural enemies against exotic stink bugs. Conservation and augmentation methods of biological control have received less attention in the US, although there may be good opportunities to utilize these approaches. We identify some considerations for the current and future use of biological control for stink bugs, including the potential for area-wide management approaches.
Capture strategies for the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), are challenging. Here we developed and evaluated a multimodal trap which combines visual and olfactory stimuli. Visual stimuli consisted of LEDs emitting UV-A and visible light. Olfactory stimuli were comprised of the synthetic aggregation pheromone and odours from trapped H. halys individuals. Stink bug attraction at different wavelengths was evaluated in laboratory two-choice bioassays, and different prototypes of the trap were tested in 2021 in natural, agricultural, and urban settings. Traps with a combination of UV-A and blue or green visible wavelengths provided higher H. halys attraction (up to ~8-fold) compared to traditional sticky or small pyramidal traps. The concurrent presence of synthetic pheromone and LED had a synergistic effect on H. halys positive phototaxis. Further development and implementation of the multimodal trap is discussed for prospective use in attract-and-kill or push–pull strategies.
Capture of stink bugs (Heteroptera: Pentatomidae) in apple orchards with yellow pyramid traps baited with Euschistus spp. (Heteroptera: Pentatomidae) aggregation pheromone, methyl (2E,4Z)-decadienoate, was 4 fold greater when traps were topped with a 3.8-L jar with a 1.6 cm diameter opening and trimmed wire edging than with a 1.9-L jar with a 5 cm diameter opening with no wire edging. Stink bug capture in the 3.8-L jar top was unaffected by the presence or size of an insecticide ear tag, indicating that this improved design led to increased captures by reducing escape. Sixty-four percent fewer stink bugs escaped from 3.8-L jar tops with the improved capture mechanism than from the 1.9-L jar tops. Green stink bug, Acrosternum hilare (Say), was more susceptible to the presence of the insecticide ear tag than the brown stink bug, Euschistus servus (Say), with dusky stink bug, E. tristigmus (Say), exhibiting high mortality in traps with and without ear tags. Among baited and unbaited pyramid traps with different visual stimuli, fewer captures were recorded in black pyramid traps than in clear, yellow, green or white pyramid traps. Similar numbers of brown stink bugs were captured in yellow pyramid traps deployed on the ground between trees or on horizontal branches within trees in the orchard border row. Captures of dusky and green stink bugs were greater in the tree pyramid, especially from August to mid-October. Relationships between stink bug capture and injury will need to be determined before this trap can be incorporated as a decision-making tool in pest management programs.
Field-based experiments were conducted to evaluate the response of the abundant brown stink bug, Euschistus servus (Say), to commercially available pheromone lures containing methyl (2E,4Z)-decadienoate deployed in association with yellow pyramid traps. Euschistus servus aggregated over a zone of at least 3.14 m2 based on significantly greater numbers located on mullein plants located 1 m from baited traps compared with plants at 5 and 10 m. At this distance, ∼96% of all adults located on mullein plants were not subsequently captured by baited traps. However, the presence of mullein plants near baited traps did not significantly reduce baited trap captures. Even if mullein plants were not present, baited trap captures remained statistically identical. Based on all adults captured in baited traps and located on surrounding mullein plants, 50% of all individuals that entered plots were captured in traps.
A regression model was developed to predict the flight activity of Acrosternum hilare (Say) using data on the number of adults collected in a single black light trap located in Painter, VA, in the 18-yr period from 1990 to 2007. Eighteen initial weather variables, including cumulative precipitation over different time periods, mean monthly precipitation (PJA) and days below freezing (DFJA) from January to April, and mean monthly temperatures from December to April were tested in developing the regression model. Mixed (backward and forward) stepwise regression analysis showed that a two-variable model using PJA and DFJA was adequate for predicting the seasonal mean weekly number of A. hilare adults in the trap. Validation of the model using five independent black light trap data sets resulted in a strong correlation (r = 0.98) between observed and predicted mean weekly number of A. hilare adults caught in traps. Three peaks in flights of A. hilare adults were observed when mean trap catch was plotted over time for the 18-yr period. Peaks occurred at 319, 892, and 1,331 degree days (DD) from 1 January. Based on known developmental rates, the first peak was attributed to overwintered adults, the second to first-generation adults, and the third to a second generation of adults. This research suggests that A. hilare undergoes two complete generations in Virginia. Cumulative trap catch estimated from the 18-yr mean trap catch showed that 10, 50, and 90% of the total seasonal catch should occur by 153, 501, and 1,066 DD.
A scintillation glass-vial bioassay was used to test technical grade insecticides against the non-native stink bug Halyomorpha halys (Stål). Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is emerging as an important pest in the Mid-Atlantic States, especially in tree fruits and as a homeowner nuisance during the winter. Pyrethroid insecticides, especially bifenthrin, caused mortality against H. halys at low doses, with LC50 values of 0.03-0.49 (microg [AI]/cm2) (mg body mass(-1)). Three nicotinoids were tested against adults with LC50 values ranging between 0.05 and 2.64 (microg [AI]/cm2) (mg body mass(-1)). Phosmet had LC50 values that were up to 3.6-fold higher than other classes of insecticides tested. Fifth instars of H. halys were evaluated against selected chemicals, and they were generally susceptible at lower rates than the adults. Due to significant differences in weight, males and females were individually weighed, tested, and analyzed separately. Sex-related differences in susceptibility were found in the responses to thiomethoxam with males being less susceptible despite having a smaller body mass.
The attraction of the stink bug Euschistus conspersus Uhler to sources of the synthetic pheromone component methyl (2E,4Z)-decadienoate was investigated in a series of field experiments in native vegetation surrounding commercial apple orchards in Washington. In experiments with pheromone lures placed inside two different tube-type traps, stink bugs were attracted to the immediate area around traps in large numbers, but very few were caught in the traps. Pheromone lures attached directly to the host plant mullein, Verbascum thapsus L., demonstrated that these 'baited" plants attracted significantly more E. conspersus than unbaited plants. Spring (reproductive) and summer (reproductively diapausing) E. conspersus adults, both males and females, were attracted to pheromone-baited plants. There was no significant difference in the number of male or female E. conspersus attracted to pheromone-baited traps or plants in any of the experiments, further characterizing methyl (2E,4Z)-decadienoate as an aggregation, and not a sex pheromone. Stink bug aggregations formed within 24-48 h of lure placement on mullein plants and remained constant until the lure was removed after which aggregations declined over 3-4 d to the level of unbaited plants. The implications of these studies for E. conspersus monitoring and management are discussed.
Pyramid traps coated with "industrial safety yellow" exterior latex gloss enamel paint and baited with Euschistus spp. aggregation pheromone, methyl (2E,4Z)-decadienoate captured more stink bugs than all other baited and unbaited trap types in both apple and peach orchards in 2002 and 2003. Commercial sources of dispensers of methyl (2E,4Z)-decadienoate deployed in association with pyramid traps had a significant impact on trap captures. Captures in pyramid traps were four-fold greater when baited with lures from IPM Technologies, Inc. (Portland, OR) than with lures from Suterra (Bend, OR). Variation in yellow pyramid trap color ("industrial safety yellow" and "standard coroplast yellow") and material (plywood, plastic, and masonite) did not affect trap captures. Brown stink bug was the predominant species captured (58%), followed by dusky stink bug, Euschistus tristigmus (Say) (20%); green stink bug, Acrosternum hilare (Say) (14%); and other stink bugs (Brochymena spp. and unidentified nymphs) (8%). Captures in baited pyramid traps were significantly correlated with tree beating samples in both managed and unmanaged apple orchards and with sweep netting samples in the unmanaged apple orchard. However, problems associated with trapping mechanisms of pyramid trap jar tops and jar traps likely resulted in reduced captures in baited traps. Improved trapping mechanisms must be established to develop an effective monitoring tool for stink bugs in mid-Atlantic orchards.
Halyomorpha halys (Stål) (Pentatomidae), called the brown marmorated stink bug (BMSB), is a newly invasive species in the eastern USA that is rapidly spreading from the original point of establishment in Allentown, PA. In its native range, the BMSB is reportedly attracted to methyl (E,E,Z)-2,4,6-decatrienoate, the male-produced pheromone of another pentatomid common in eastern Asia, Plautia stali Scott. In North America, Thyanta spp. are the only pentatomids known to produce methyl 2,4,6-decatrienoate [the (E,Z,Z)-isomer] as part of their pheromones. Methyl 2,4,6-decatrienoates were field-tested in Maryland to monitor the spread of the BMSB and to explore the possibility that Thyanta spp. are an alternate host for parasitic tachinid flies that use stink bug pheromones as host-finding kairomones. Here we report the first captures of adult and nymph BMSBs in traps baited with methyl (E,E,Z)-2,4,6-decatrienoate in central Maryland and present data verifying that the tachinid, Euclytia flava (Townsend), exploits methyl (E,Z,Z)-2,4,6-decatrienoate as a kairomone. We also report the unexpected finding that various isomers of methyl 2,4,6-decatrienoate attract Acrosternum hilare (Say), although this bug apparently does not produce methyl decatrienoates. Other stink bugs and tachinids native to North America were also attracted to methyl 2,4,6-decatrienoates. These data indicate there are Heteroptera in North America in addition to Thyanta spp. that probably use methyl 2,4,6-decatrienoates as pheromones. The evidence that some pentatomids exploit the pheromones of other true bugs as kairomones to find food or to congregate as a passive defense against tachinid parasitism is discussed.
Identification of the aggregation pheromone responsible for the aggregation phenomena of the brown-winged green bug, Plautia stali SCOTT (Heteroptera: Pentatomidae) was attempted. Volatiles collected from adult males which attracted adults showed attraction activity under field conditions. Volatiles were then collected from a total of 180,000 adult males and the activity of the fractionated samples was field tested using water pan traps. A mixture of hexane and 5% ether in hexane fractions from Florisil LC showed attraction activity, and this was further purified with HPLC and GC. By GC-MS and NMR analysis (COSY), the chemical structure of the active compound was identified as methyl (E,E,Z)-2,4,6-decatrienoate. The attraction activity of the synthesized compound of this structure was confirmed by field tests.
Field studies were conducted to evaluate the effectiveness of an improved pyramidal trap for monitoring fruit-piercing stink bugs such as Plautia crossota stali Scott, Halyomorpha halys (Stal), and Glaucias subpunctatus (Walker) in two regions with different stink bug population densities. Improved traps, made from either yellow or translucent and colorless materials, were compared with the original pyramidal trap and the standard water-basin trap. All traps were baited with P. c. stali aggregation pheromone. The translucent, colorless trap captured significantly more target insects than the original design or the yellow trap, although there was no significant difference in one region. Further, the translucent improved design trap caught stink bugs comparable to the water-basin trap, and fluctuations in capture of P. c. stali were proportionally similar between the two trap types. The improved trap design eliminates the need for changing water in the standard water-basin trap, thus the improved trap may be used as an effective and simple monitoring tool over a wide geographical range.
The knockdown and lethal efficacies of five aerosol formulations including Combat Speed® (AIs: 0.1 % imiprothrin and 0.3% cyphenothrin), Raid Power® (AIs: 1.0% pyrethrin and 0.2% permethrin), Home Keeper®, (AIs: 0.2% tetramethrin and 0.3% permethrin), Super Killer® (AIs: 0.32% tetramethrin and 0.08% bioresmethrin), and Perma Kill-K® (AIs: 0.3% dichlorvos and 0.1% tetramethrin) against five strains of the German cockroach, Blattella germanica (L.) were assessed. The results show that the mean value of KT50 (5.4 sec.) of Combat Speed® was 4.5 and 3.1-folds lower than those of Perma Kill-K® and Home Keeper®, respectively. The mean value of KT90 (9.0 sec; slope = 10.02) of Combat Speed® was 3.8 to 5.8-folds lower than Perma Kill-K®, Supper Killer® and Home Keeper®. As lethal effects, the mean value of LT50 (17.3 sec.) of Combat Speed® was over 26 folds lower than Supper Killer® and Perma Kill-K®. The mean value of LT90 (32.9 sec.) of Combat Speed® was 37.4 and 15.1-folds lower than those of Supper Killer® and Perma Kill-K®, respectively. In general, Combat Speed® and Raid Power® were considered the insecticide aerosols with faster knockdown and higher lethal effects than Supper Killer®, Perma Kill-K®, and Home Keeper® against five strains of German cockroaches in Korea. Also, the knockdown and lethal effects of Supper Killer®, Perma Kill-K®, and Home Keeper® were highly variable depends on the strains.