Spatiotemporal distribution of the hemlock woolly adelgid predator Laricobius nigrinus after release in eastern hemlock forests

• 1 Post‐release distributions of Laricobius nigrinus, a biological control predator of hemlock woolly adelgid Adelges tsugae Annand, were evaluated at eight hemlock forests in the eastern U.S.A.
• 2 Vertical dispersal of F₁ and F₂L. nigrinus were assessed from within three crown strata (<7, 7–15 and >15 m) at four release sites.
• 3 Horizontal distributions of L. nigrinus within the forest surrounding central release areas were observed in two separate studies, which included (i) release and monitor to capture parent and F₁ movement by sampling the immature life stages of the offspring, and (ii) assessment of F₃ to F₆ generations where beetles were previously determined to be established.
• 4 Laricobius nigrinus, released on lower crown branches, oviposited within the upper crown stratum and were slow to disperse from release trees. Monitoring L. nigrinus only from the lower crown would likely underestimate its presence because 86% of the F₂ generation were detected above 15 m.
• 5 By the fifth generation, the frequency distributions of larvae increased at increasing distance from release areas; larvae were recovered at a maximum distance of approximately 400 m and the spread rate was approximately 39 m/year.
• 6 Slow dispersal of L. nigrinus and uninterrupted recovery of six generations in the presence of fluctuating prey density support its continued release as part of the A. tsugae biological control programme. These data contribute toward improved release strategies and monitoring for this biological control agent.

     

Establishment and coexistence of two predators,Laricobius nigrinus and Sasajiscymnus tsugae,introduced against hemlock woolly adelgid on eastern hemlock

The coexistence of two introduced predatory species, Laricobius nigrinus Fender and Sasajiscymnus tsugae (Sasaji and McClure), and a native predator, L. rubidus LeConte, on eastern hemlock was documented for the first time. Details of their coexistence and implications to management of hemlock woolly adelgid, Adelges tsugae Annand, are discussed.     

Orientation behavior of the predator Laricobius nigrinus (Coleoptera: Derodontidae) to hemlock woolly adelgid and host tree odors in a multi-chambered olfactometer

We studied the adult ambulatory response of the predator, Laricobius nigrinus Fender (Coleoptera: Derodontidae), to odors from its prey, Adelges tsugae Annand, the hemlock woolly adelgid, and foliage of hemlock woolly adelgid, host hemlocks (Tsuga spp.), and other conifers. Both the predator and hemlock woolly adelgid are apparently native to western North America, but the predator is being released in the eastern United States, which has different hemlock species, for biological control of a lineage of hemlock woolly adelgid inadvertently introduced from Japan. L. nigrinus responded to odors from hemlock woolly adelgid host trees, but not to odors from hemlock woolly adelgid. L. nigrinus collected from hemlock woolly adelgid-infested western hemlock were more strongly attracted to odors from western hemlock [Tsuga heterophylla (Rafinesque) Sargent] than eastern hemlock [Tsuga canadensis (L.) Carrière] in most trials. Odors from western white pine (Pinus monticola Douglas ex D. Don) and white spruce [Picea glauca (Moench) Voss] were as attractive as western hemlock odors whereas odors from Douglas-fir [Pseudotsuga menziesii variety menziesii (Mirbel)] and ponderosa pine (Pinus ponderosa Douglas ex Lawson) were avoided. L. nigrinus reared on hemlock woolly adelgid-infested eastern hemlock in the laboratory were lethargic and were not attracted to either eastern or western hemlock odors. Predators collected in the field and tested monthly from December to March responded similarly each month, except February, when they flew rather than walked in the olfactometer, suggesting a period of dispersal or mate finding at that time of year. The implications of these results for programs to release L. nigrinus in the eastern United States for control of hemlock woolly adelgid are discussed.     

Assessment of the potential for hybridisation between Laricobius nigrinus (Coleoptera: Derodontidae) and Laricobius osakensis,predators of the hemlock woolly adelgid (Hemiptera: Adelgidae)

In 2003, Laricobius nigrinus Fender was introduced into the eastern United States as a biological control agent of the hemlock woolly adelgid (Adelges tsugae Annand). Following its release, it was discovered that L. nigrinus was hybridising and producing viable progeny with Laricobius rubidus LeConte, a species native to eastern North America. Recently, Laricobius osakensis Montgomery and Shiyake was imported from Japan into the USA as a potential biological control agent of hemlock woolly adelgid. Hybridisation between L. nigrinus and L. rubidus led to interest in the outcome of interactions between L. osakensis and the other two Laricobius spp. The purpose of this study was to determine if L. osakensis could mate with L. nigrinus, if they could produce hybrid progeny, and whether mating interferes with reproductive output. Laricobius spp. were observed mating directly following emergence and found to be capable of producing sterile eggs in the absence of a mating event. Laboratory and confined field studies found no evidence that L. osakensis and L. nigrinus could produce hybrid progeny and the interaction between the two species did not result in a lower reproduction associated with interspecific mating attempts. Interbreeding should therefore not have an impact on biological control using these species. Fecundity experiments showed that L. osakensis produced eggs earlier in the season and at a higher rate than L. nigrinus, suggesting that L. osakensis may have the potential to be an even more successful biological control agent than L. nigrinus.     

Survival and reproduction of Laricobius nigrinus Fender (Coleoptera: Derodontidae), a predator of hemlock woolly adelgid,Adelges tsugae Annand (Homoptera: Adelgidae) in field cages

Laricobius nigrinus Fender (Coleoptera: Derodontidae) is being evaluated as a biological control agent for the hemlock woolly adelgid (HWA), Adelges tsugae Annand (Homoptera: Adelgidae). Predator exclusion studies on survival, reproduction, and impact on HWA populations were investigated over two years in Virginia, US. In year 1, branches were selected to receive one of three treatments: caged hemlock branches with predators; caged hemlock branches without predators; and uncaged hemlock branches. L. nigrinus adults survived from February to April, producing up to 41 progeny per female. Adelgid densities on branches exposed to L. nigrinus exhibited a significantly higher rate of decline than those on branches not exposed to predators. Additionally, the final density of sistens and progrediens was significantly lower on caged branches containing L. nigrinus than on caged and uncaged branches without predators. In year 2, L. nigrinus survival and predation was evaluated over two 10-week sample periods: (November–January and February–April). L. nigrinus survived throughout the 6-month test period, with 89% surviving through January and 55% through April. Between February and April, 38 progeny were produced per beetle. The decrease in adelgids, measured in both numbers of adelgids and percent reduction per branch, was significantly higher (p < 0.0001) on caged branches with L. nigrinus than on those without predators.     

Development and reproductive biology of Laricobius nigrinus, a potential biological control agent of Adelges tsugae

Biological studies on Laricobius nigrinus Fender (Coleoptera: Derodontidae) were conducted in the laboratory to obtain basic information on this littleknown predator. Laricobius nigrinus is acandidate biological control agent of thehemlock woolly adelgid, Adelges tsugaeAnnand (Homoptera: Adelgidae), an exotic peston eastern (Tsuga canadensis (L.)Carrière) and Carolina (T.caroliniana Engelmann) hemlocks in the easternUnited States. It is univoltine andundergoes an aestival diapause. Post-aestivation activity period was 36.6 and30.8 weeks for males and females, respectively. Adult activity and oviposition are wellsynchronized with the over-wintering generationof A. tsugae. Mean lifetime fecunditywas 100.8 eggs over a mean duration of 13.2weeks oviposition period. Within thetemperature range (12–18°C) studied,development was fastest at 18°C. Meandevelopment time from egg to adult was 88.8,64.8 and 46.6 days at 12, 15 and 18°C,respectively. Laricobius nigrinus hasfour larval instars. Mean larval consumptionwas 225.9 and 252.3 A. tsugae eggs at 12and 18°C, respectively. Thesefindings provide essential data on the rate ofdevelopment and feeding capacity of L. nigrinusat temperatures typical of ambientconditions during late winter/early spring inVirginia. Its rapid development at18°C indicates that it has potential asa biological control agent of A. tsugaebecause of its synchrony with the developmentof the over-wintering generation of A. tsugaein eastern United States.     

Competitive interactions among two specialist predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae) in south-western Virginia

1 Competitive interactions among two specialist predators, Laricobius nigrinus and Sasajiscymnus (Pseudoscymnus) tsugae, and a generalist predator, Harmonia axyridis Pallas, of hemlock woolly adelgid, Adelges tsugae were evaluated in hemlock stands in south‐western Virginia. The two specialist predators are part of a biological control program for A. tsugae, and the potential for competition among these species and previously established generalist predators in the field is unknown. 2 Adult predators were evaluated in branch cages during spring and summer at two field sites infested with A. tsugae. Using females only in 2003 and sexual pairs in 2004, predator survival and net reproduction were examined, as well as their feeding and impact on A. tsugae when present alone and in conspecific and heterospecific groupings. 3 Predator survival was not affected by the presence of additional predators. Total feeding was greater for all species when placed in predator groupings, suggesting that interactions do not significantly interfere with feeding activity. Net reproduction per predator was negatively affected by conspecifics, but unaffected by heterospecifics, indicating that direct or indirect intraspecific interference may occur. In spring, L. nigrinus showed the greatest impact on A. tsugae, and H. axyridis had the greatest impact during summer. 4 These results suggest that it would be beneficial to utilize multiple predator species combinations over single species when implementing biological control for A. tsugae. Low‐density releases are also recommended to reduce intraspecific interference.     

Volatile emissions of eastern hemlock,Tsuga canadensis,and the influence of hemlock woolly adelgid

The volatile emissions of eastern hemlock, Tsuga canadensis Carriere, were identified and quantified using standard and chiral gas chromatography and mass spectrometry. All of the identified compounds were monoterpenes, and included alpha-pinene, myrcene, tricyclene, camphene, alpha-phellandrene, beta-pinene, limonene, beta-phellandrene, terpinolene, and bornyl acetate. alpha-Pinene, myrcene, and camphene comprised greater than 75% by mass of the total release. Infestation by the exotic insect, hemlock woolly adelgid (HWA, Adelges tsugae Annand), resulted in an increased release rate of monoterpenes from branch tips. Release rate was negatively correlated to the amount of the branch tip sample that was new growth, suggesting that release rate is greater from previous-year foliage. Additionally the percent composition of the volatile profile is slightly altered by infestation, with alpha-pinene comprising 57% of volatiles from infested foliage and 66% from uninfested foliage.     

Anisotropic spread of hemlock woolly adelgid in the eastern United States

Simple population models predict that the spread of an invading species through a homogenous habitat should be equal in all directions, but geographic variation in the habitat that affects either reproduction or movement could result in variable rates of spread. We analyse records of the historical range expansion of the hemlock woolly adelgid (HWA) (Adelges tsugae Annand) in the eastern United States from 1951 to 2006 to document that this species has spread in an anisotropic fashion. Furthermore, the magnitude and direction of this anisotropy has varied through time. We explore the extent to which this spatial and temporal variation in spread can be explained by geographical variation in climate and by the abundance of hosts, eastern hemlock (Tsuga canadensis L.) and Carolina hemlock (Tsuga caroliniana Engelm.). We found that a significant component of the spatial anisotropy in HWA spread rate can be explained by the geographical distribution of host trees. January temperatures were negatively associated with spread rates but this may be an artifact of the association between hemlock and cold climates. The current distribution of the adelgid in eastern N. America may be approaching the extent of its potential range to the south and west determined by availability of host hemlock and to the north determined by lethal cold winter temperatures.     

Simulating the dispersal of hemlock woolly adelgid in the temperate forest understory

The hemlock woolly adelgid (HWA), Adelges tsugae Annand (Hemiptera: Adelgidae), has spread rapidly across the eastern USA since its introduction from Japan 60 years ago, causing widespread mortality of both eastern hemlock [Tsuga canadensis (L.) Carrière] and Carolina hemlock [Tsuga caroliniana Engelm. (Pinaceae)]. Although HWA spread patterns have been repeatedly analyzed at regional scales, comparatively little is known about its dispersal potential within and between hemlock stands. As the small size and clonal nature of HWA make it nearly impossible to identify the source populations of dispersing individuals, we simulated intra‐stand HWA movement in the field by monitoring the movement of clumps of fluorescent powder that are slightly larger than HWA, but much easier to detect in the forest understory. Using three hemlock trees with three colors of fluorescent powder as source populations, we detected dispersal events at the farthest distances within our trapping array (400 m). However, more than 90% of dispersal events were <25 m. Dispersal patterns were similar from all three source trees and the distribution of dispersal distances in all cases could be described by lognormal probability density functions with mean dispersal distance of 12–14 m, suggesting that dispersal was relatively independent of location of source trees. In general, we documented tens of thousands of passive dispersal events in the forest understory despite the presence of a dense forest canopy. Thus, even under relatively light‐wind conditions, particles of similar dimensions to HWA are capable of intra‐stand movement, suggesting that a large population of HWA could rapidly infest other trees within several hundred meter radius, or beyond.     

铁杉球蚜的生物学及空间分布

通过对铁杉(Tusga chinensis Pritz)-云杉(Picea retroflexac Mast)、铁杉-华山松(Pinus armardi Franch)、云南铁杉(Tusga domosa Eichler)-槭树(Acer mono Maxim)-桦木(Betula platyphylla Suk)四川主要铁杉林类型中铁杉球蚜Adelges tsugae Annand林间定株、种群随机抽样、室内饲养研究表明,铁杉球蚜在四川1年发生2代(越冬代和第1代),世代重叠,成虫营孤雌生殖。越冬代从4月上旬至第2年的4月下旬,产卵盛期在5月下旬,平均产卵量为15.58粒,1龄若虫具有滞育越夏习性;第1代从12月下旬至8月中旬,产卵盛期在3月下旬,平均产卵量为67.37粒,并可产生有翅成虫,但无转主危害现象。种群的发育与温度有相关性,温度高林分种群发育进度快于温度低林分。该虫的危害与生境有一定相关性,铁杉针阔混交林危害重于铁杉针叶林;同一树冠不同层次之间、不同方位之间危害程度差异不显著;当年受害严重的树株第2年受害不严重。     

Factors affecting settlement rate of the hemlock woolly adelgid,Adelges tsugae,on eastern hemlock,Tsuga canadensis

1 We assessed the importance of several factors potentially affecting the settlement rate of the invasive hemlock woolly adelgid Adelges tsugae (Hemiptera: Adelgidae) on uninfested foliage of the eastern hemlock, Tsuga canadensis. We conducted our experiments in Massachusetts (U.S.A.) with overwintering sistens adelgids, and applied standard densities of infested foliage to uninfested branches in a planned multiple‐comparison design. 2 Settlement rates of progrediens crawlers produced by the overwintering sistens were highest when adelgid‐infested foliage was loosely attached to uninfested foliage and both branches were then enclosed in a mesh sleeve. 3 Early‐emerging crawlers settled at a higher rate than did late‐emerging crawlers. 4 Increasing the density of infested branches did not affect settlement rates. 5 We also tested whether less severe winter conditions improved settlement, and found that overwintering infested foliage in a refrigerator decreased settlement rate relative to foliage overwintered outdoors. 6 Our results suggest a protocol for adelgid inoculations that could substantially increase the success rate of experimental manipulations and encourage additional research on the population dynamics of this pest.     

Recovery of Sasajiscymnus tsugae,released against hemlock woolly adelgid,Adelges tsugae,in the southern Appalachians

Eastern hemlock in the Great Smoky Mountains National Park is currently threatened by the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae). As part of a management plan against this invasive insect pest, about 350,000 adults of the predatory beetle Sasajiscymnus tsugae (Sasaji and McClure) (Coleoptera: Coccinellidae) were released at ca. 150 sites in the Park from 2002 to 2007. Of these adult release sites, 33 were sampled in 2008 and 2009 using beat-sheet sampling for 4 man-hours. Sasajiscymnus tsugae adults (n=78) and/or larvae (n=145) were recovered from seven sites (21.2% of the release sites sampled). Recovery of S. tsugae was significantly associated with older release sites, with the most beetles recovered from 2002 release sites. These results indicate that S. tsugae may require more time (i.e., 5–7 years) than anticipated for population densities to reach readily detectable levels in some areas.     

Development and feeding of <Emphasis Type="Italic">Tetraphleps galchanoides</Emphasis>, a predator of the hemlock woolly adelgid

Tetraphleps galchanoides Ghauri (Hemiptera: Anthocoridae) nymphs were collected from hemlock woolly adelgid (HWA) Adelges tsugae Annand (Hemiptera: Adelgidae) infested Tsuga sp. in Baoxing, Sichuan, China. First and second stage nymphs collected from foliage shipped from China; were reared to adults and tested for feeding rates and host preferences. They were reared at 5, 8, 12, and 15 ± 1 °C from November to December, January to March, April, and May to June, respectively, in the quarantine laboratory at Virginia Polytechnic Institute and State University. At 8 °C, development time was 15, 20, and 40 days for the N-III, IV, and V nymphal stages, respectively. Adult males lived 83 days with a range of 21–147 days. A single adult female lived for 21 days. At 5 °C, second stage T. galchanoides nymphs consumed 0.8 HWA nymphs per day, and 2.0 HWA nymphs per day at the N-V stage. At 8 °C, consumption of HWA nymphs ranged from 1.3 to 3.4 nymphs per day for the N-III to N-V stages, respectively. Adult T. galchanoides consumed more HWA eggs than HWA adults, pine bark adelgid (PBA) Pineus strobi (Hartig) (Hemiptera: Adelgidae) adults, and eggs in no-choice tests. In choice tests with HWA eggs and PBA eggs, more HWA eggs were eaten. Adult and nymph body measurements are presented for determination of nymphal instars.     

Changes in the regional abundance of hemlock associated with the invasion of hemlock woolly adelgid (Adelges tsugae Annand)

Since its introduction, the non-native hemlock woolly adelgid (Adelges tsugae) has spread to infest hemlock (Tsuga spp.) in at least 18 states in the eastern USA. Previous studies have documented highly variable rates of hemlock mortality among infested stands making it difficult to estimate regional impacts. Here data from the US Forest Service Forest Inventory and Analysis program collected from 432 eastern U.S. counties reveals several surprising and conflicting regional patterns. First, median live and dead hemlock basal area has generally increased over the last two decades across the eastern U.S. This has generally been the case in both infested and uninfested counties. Second, the median percentage of hemlock which is alive has decreased over the past ~20 years, again in both infested and uninfested counties. Third, the ages of infestations are negatively correlated with the percentage of live hemlock, as might be expected given the known impact adelgids can have on a stand through time; however this relationship depends on the exclusion of uninfested counties, as counties infested >12 years and uninfested counties have similar percentages of live hemlock. Combined, these data suggest increasing tree density associated with the past century of reforestation and succession in the eastern U.S. may currently be overwhelming the negative impacts of the adelgid at the regional scale, however, the long-term stability of this situation is not known, and data from long-infested counties suggest the landscape may be at a “tipping point”.     

Seasonal synchrony of life cycles between the exotic predator,Pseudoscymnus tsugae (Coleoptera: Coccinellidae) and its prey,the hemlock woolly adelgid Adelges tsugae (Homoptera:Adelgidae)

1 The seasonal synchrony between the exotic predator, Pseudoscymnus tsugae and its prey, the hemlock woolly adelgid, Adelges tsugae, was investigated in field cages and in the forest in Connecticut, U.S.A. from 1997–1999. 2 In early spring, egg to adult development took 45 d at 18.7 °C, 39.7 d at 20.2 °C and 31.5 d at 22.7 °C. Earliest emerging F1 adults mated and oviposited in the same year. whereas F1 and F2 females emerging later in the summer mated and reserved most of their egg complement for the following year. 3 A second generation of P. tsugae is possible in Connecticut but may be delayed by cool mid‐spring temperatures. Individuals of three generations of P. tsugae, including overwintering survivors, may coexist in July and August and adults can be found year‐round with A. tsugae in infested hemlock forests. 4 A linear regression model for development from egg to adult under field temperatures gave good agreement with results from constant temperature findings. The model predicted a lower development threshold of 9.5 °C and a sum of effective temperatures of 405 day °C. Development time of P. tsugae is shorter relative to its prey A. tsugae and generation time ratios of predator to prey was 0.16–0.5, with an advantage conferred on the coccinellid. 5 Overwintering ability and behaviour were determined in 1998–1999 and adults remained on infested hemlock branches throughout a mild winter, becoming reproductively active in mid‐April. Peak oviposition period extended from April to July, in synchrony with peak oviposition and developing stages of two generations of A. tsugae.     

Activity and residues of imidacloprid applied to soil and tree trunks to control hemlock woolly adelgid (Hemiptera: Adelgidae) in forests

We studied imidacloprid application methods and timing to control the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), in forests. The methods compared were 1) soil injection near the trunk; 2) soil injection dispersed throughout the area under the canopy; 3) soil drench near the base of the trunk; and trunk injection with the 4) Arborjet, 5) Wedgle, and 6) Mauget systems. The applications were made in the fall and the following spring. Adelgid populations on the hemlocks (Tsuga spp.) were assessed in the fall of two successive years after the treatments. Relative to the untreated control trees, all the soil applications resulted in population reductions, but none of the trunk injections resulted in reductions. Fall and spring treatment efficacy did not differ. Reductions by the soil treatments were between 50 and 100% (avg 80%) by the first fall and 83-100% (avg 98.5%) by the second fall. Analysis of imidacloprid residues using enzyme-linked immunosorbent assay found residues in sap, needles, and twigs 1 mo to 3-yr after application. A laboratory dose-response bioassay using excised, adelgid-infested hemlock branches with cut ends immersed in serial dilutions of imidacloprid determined the LC50 value to be 300 ppb, based on an exposure of 20 d. A high degree of suppression of the adelgid on forest trees was associated with residues in hemlock tissue > 120 ppb 2 yr after soil treatment. Although precise relationships between residues and efficacy are elusive, it is clear that soil application of imidacloprid resulted in chronic residues of imidacloprid in tissues and suppression of adelgid populations for > 2 yr.     

The big chill: quantifying the effect of the 2014 North American cold wave on hemlock woolly adelgid populations in the central Appalachian Mountains

The ability to survive winter temperatures is a key determinant of insect distributional ranges and population dynamics in temperate ecosystems. Although many insects overwinter in a state of diapause, the hemlock woolly adelgid [Adelges tsugae (Annand)] is an exception and instead develops during winter. We studied a low density population of A. tsugae, which undergoes two generations per year, in a forested area in which its only available host plant, eastern hemlock (Tsuga canadensis), was patchy and scarce. In January 2014, this area also experienced an exceptionally cold winter due to a southward shift in the North Polar Vortex. We used 3 years of systematic sampling prior to the 2014 cold wave, and 1 year following, to quantify the effect of the 2014 cold wave on A. tsugae population dynamics. We observed a strong negative correlation between the number of days below sub-zero temperature thresholds and A. tsugae, and estimated that the 2014 cold wave resulted in at least a 238% decrease in its population growth rate. However, we also observed that the detrimental effect of the 2014 cold wave to A. tsugae was short-lived, as populations measured in the late summer of 2014 rebounded to pre-2014 cold wave densities. This study highlights the effect that cold winter weather events can have on a winter active insect species, and the speed at which populations can recover from stochastic mortality events.     

Factors influencing the abundance of Trioxys pallidus,a successful introduced biological control agent of walnut aphid in California

This field study reports on factors influencing the abundance of Trioxys pallidus 35 years after its successful introduction in California, and in the presence of continued hyperparasitism and intraguild predation. The seasonal activity of Chromaphis juglandicola and T. pallidus were monitored in 2005–06 in relation to hyperparasitism and mummy predation in three orchards. Walnut aphids remained under the economic threshold in all three orchards with insecticide treatments for other pests in some cases reducing aphid populations as well. No significant density-independent or density-dependent aggregation in the risk of hyperparasitism was found at the individual tree scale, suggesting the absence of a refuge from hyperparasitism. In contrast, significant negative density-dependent aggregation in the risk of intraguild predation was found, but no density-independent aggregation, suggesting a refuge at higher mummy densities. Using a linear mixed effects model, the following factors were found to influence mummy density: aphid density from the previous sample date and intraguild predation, with the latter linked to hyperparasitism from the previous sample date through a significant interaction that appears to be mediated by current aphid density.