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.     

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.     

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.     

Hybridization between a native and introduced predator of Adelgidae: An unintended result of classical biological control

Hybridization between introduced biological control agents and native species has the potential to impact native biodiversity and pest control efforts. This study reports progress towards predicting the outcome of hybridization between two beetle species, the introduced Laricobius nigrinus Fender and the native L. rubidus LeConte. L. nigrinus is a predator from western North America introduced to hemlock stands in the eastern United States as a biological control of the hemlock woolly adelgid [Adelges tsugae Annand (Hemiptera: Adelgidae)]. Laricobius rubidus is a closely related eastern species that also feeds on A. tsugae but prefers pine adelgids (Pineus strobi Hartig) on white pine (Pinus strobus L.). Six microsatellite markers plus mitochondrial COI haplotypes were used to examine genetic structure of these two Laricobius species across North America. In their native ranges, major geographic features have impacted gene flow: the intermountain region in the West, and the Appalachian Mountains in the East. Analysis of 1229 individuals from adelgid-infested hemlock trees in release sites in the eastern United States found widespread hybridization with asymmetrical introgression towards L. nigrinus on hemlock. The ultimate outcome of hybridization could therefore be a complex mosaic of genetic introgression across the landscape, depending on the distribution of hemlock and pine. This study confirms the importance of evaluating the potential for introduced biological control agents to hybridize with their native relatives. This system also provides an excellent opportunity to improve our understanding of emerging hybrid zones by tracking its progress over time.     

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.     

Field assessment of hybridization between Laricobius nigrinus and L. rubidus,predators of Adelgidae

Two adelgid predators, Laricobius nigrinus Fender and Laricobius rubidus LeConte, were recently discovered to produce hybrid progeny in the eastern United States. L. rubidus is native to eastern North America where it feeds on pine bark adelgid (Pineus strobi Hartig) and L. nigrinus is native to western North America and was introduced to the eastern United States in 2003 for biological control of hemlock woolly adelgid (Adelges tsugae Annand). Currently, L. nigrinus and L. rubidus form a mosaic of hybrid zones throughout the eastern United States. It is not known whether these zones will be maintained over time and whether hybridization will impact the efficacy of biological control or result in displacement of L. rubidus. Sampling from 2007 to 2012 on eastern hemlock (Tsuga canadensis Carrière) showed a clear increase in L. nigrinus, a decrease in L. rubidus, and a steady proportion of hybrids. Sampling from 2010 to 2012 on both eastern hemlock and white pine (Pinus strobus L.) at ten sites showed that L. nigrinus was more dominant on hemlock and L. rubidus was more dominant on white pine, which may demonstrate habitat preference and promote segregation between the two species. Site factors were tested for a relationship with the proportion of hybrids. The number of years L. nigrinus had been present at the site was the only factor that showed a relationship. The results suggest that L. nigrinus may displace L. rubidus on hemlock, but not on white pine at sites where they are both present.     

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.     

Biology and development of <Emphasis Type="Italic">Laricobius kangdingensis</Emphasis> Zilahi-Balogh and Jelínek,a newly discovered predator of <Emphasis Type="Italic">Adelges tsugae</Emphasis>

The biology and temperature-dependent development of Laricobius kangdingensis Zilahi-Balogh and Jelínek (Coleoptera: Derodontidae), a newly described predator of hemlock woolly adelgid (HWA), Adelges tsugae Annand (Hemiptera: Adelgidae) were investigated and compared with a related HWA predator, L. nigrinus Fender, that has already been released. As with other Laricobius species, there are four larval instars. The female to male sex ratio was 1:1.1. Mean lifetime fecundity per female was 196.4 eggs and 97.9 eggs for the parental generation (P₁) and first filial generation (F₁), respectively. Developmental rates at 6, 9, 12, 15, and 18°C were studied between fall 2002 and spring 2004 and used to determine low temperature development thresholds for the egg (2.8°C), and larval (1.6°C) stages. The egg and larval thresholds are lower than those observed for L. nigrinus. Laricobius kangdingensis individuals completed development only at 12 and 15°C; however, the adults did not emerge from aestivation after pupation. Our results suggest that L. kangdingensis may be a promising addition to the complex of predators currently being reared for control of HWA. Laricobius kangdingensis is long-lived, exhibits high fecundity, and can complete development on North American HWA. However, further studies will be necessary to secure its clearance for release, and the source of high mortality in the laboratory must be identified in order to improve its survival for mass-rearing. Handling editor: Eric Lucas     

Using dendrochronology to model hemlock woolly adelgid effects on eastern hemlock growth and vulnerability

This study examined the relationship between eastern hemlock (Tsuga canadensis (L.) Carr.) crown condition and changes in radial growth associated with infestation by hemlock woolly adelgid Adelges tsugae (Homoptera: Adelgidae) (HWA). Tree-ring chronologies of eastern hemlock were used to develop a binomial decline index based on three consecutive years of below average growth. Radial growth decline was modeled, using logistic regression, as a function of an extensive array of tree, crown, and site variables that were collected over an 11 year period in Delaware Water Gap National Recreation Area. Some site-related variables such as site-location and aspect were significantly related to decline probabilities when considered individually. However, the total proportion of response variance accounted for was low, and the only site variable included in the final model was mean plot-level HWA infestation level. For every 1% increase in mean percent HWA infestation per plot, there was an 8% increase in the likelihood that a tree would be classified as being in decline. Tree crown variables such as live crown ratio, crown density, and the modified ZB_adj index, a combination of foliage transparency and branch dieback, had the most explanatory power, both individually and in the final model. These crown variables were relatively accurate predictors of the degree of hemlock growth decline during HWA infestation.     

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.     

Effects of voltinism, interspecific competition and parasitism on the population dynamics of the hemlock scales, Fiorinia externa and Tsugaspidiotus tsugae (Homoptera: Diaspididae)

Abstract.

• 1 Life tables were constructed for solitary and coexisting populations of univoltine Fiorinia externa Ferris and bivoltine Tsugaspidiotus tsugae (Marlatt) (Homoptera: Diaspididae), two exotic scale pests of eastern hemlock, Tsuga canadensis Carriere, in the northeastern United States.
• 2 Solitary and coexisting populations of F. externa had similar survivorship and population growth rates resulting in an annual increase in density of 7–16%. Survivorship of solitary and coexisting populations of T. tsugae also was similar, but growth rates differed substantially. While solitary populations increased their density by 68% annually, populations coexisting with F. extema were reduced 74% each year.
• 3 The annual reduction in T. tsugae density where it coexists with F. externa was due in part to interspecific competition which resulted in higher mortality to nymphs from dispersal and starvation and in lower fecundity of adult females relative to solitary populations. A host shift by the parasitoid, Aspidiotiphagus citrinus (Crawford) (Hymenoptera: Aphenlinidae) from F. externa to T. tsugae in autumn also accounted for 71% of the annual decrease in T. tsugae numbers. Therefore, F. externa adversely affects the growth of T. tsugae populations not only because of its superior competitive ability but also because adult para-sitoids which emerge from it subsequently attack nymphs of T. tsugae in autumn.
• 4 Parasitism and starvation of nymphs resulting from competition were the key mortality factors in the population dynamics of these exotic hemlock scales.

     

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.     

Facilitation between invasive herbivores: hemlock woolly adelgid increases gypsy moth preference for and performance on eastern hemlock

1. Interactions between invertebrate herbivores with different feeding modes are common on long-lived woody plants. In cases where one herbivore facilitates the success of another, the consequences for their shared host plant may be severe. Eastern hemlock (Tsuga canadensis), a canopy-dominant conifer native to the eastern U.S., is currently threatened with extirpation by the invasive stylet-feeding hemlock woolly adelgid (Adelges tsugae). The effect of adelgid on invasive hemlock-feeding folivores remains unknown. 2. This study evaluated the impact of feeding by hemlock woolly adelgid on gypsy moth (Lymantria dispar) larval preference for, and performance on, eastern hemlock. To assess preference, 245 field-grown hemlocks were surveyed for gypsy moth herbivory damage and laboratory paired-choice bioassays were conducted. To assess performance, gypsy moth larvae were reared to pupation on adelgid-infested or uninfested hemlock foliage, and pupal weight, proportional weight gain, and larval period were analysed. 3. Adelgid-infested hemlocks experienced more gypsy moth herbivory than did uninfested control trees, and laboratory tests confirmed that gypsy moth larvae preferentially feed on adelgid-infested hemlock foliage. Gypsy moth larvae reared to pupation on adelgid-infested foliage gained more weight than larvae reared on uninfested control foliage. 4. These results suggest that the synergistic effect of adelgid and gypsy moth poses an additional threat to eastern hemlock that may increase extirpation risk and ecological impact throughout most of its range.     

Competitor avoidance drives within‐host feeding site selection in a passively dispersed herbivore

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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.     

Predators associated with the hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest

The hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), is causing widespread mortality of eastern hemlock, Tsuga canadensis L. Carrière, in the eastern United States. In western North America, feeding by A. tsugae results in negligible damage to western hemlock, Tsuga heterophylla (Raf.) Sargent. Host tolerance and presence of endemic predators may be contributing to the relatively low levels of injury to T. heterophylla caused by A. tsugae. Field surveys of the predator community associated with A. tsugae infestations on 116 T. heterophylla at 16 sites in Oregon and Washington were conducted every 4-6 wk from March 2005 through November 2006. Fourteen uninfested T. heterophylla were also surveyed across 5 of the 16 sites. Each sample tree was assigned an A. tsugae population score ranging from 0 to 3. Predators collected from A. tsugae-infested T. heterophylla represent 55 species in 14 families, listed in order of abundance: Derodontidae, Chamaemyiidae, Hemerobiidae, Coccinellidae, Cantharidae, Reduviidae, Miridae, Syrphidae, Chrysopidae, Coniopterygidae, Staphylinidae, Anthocoridae, Nabidae, and Raphidiidae. Laricobius nigrinus Fender (Coleoptera: Derodontidae), Leucopis argenticollis Zetterstedt (Diptera: Chamaemyiidae), and Leucopis atrifacies (Aldrich) (Chamaemyiidae) were the most abundant predators; together comprising 59% of predator specimens recovered. Relationships among predators and A. tsugae were determined through community structure analysis. The abundances of Laricobius spp. larvae, L. nigrinus adults, Leucopis spp. larvae, and L. argenticollis adults were found to be positively correlated to A. tsugae population score. Predators were most abundant when the two generations of A. tsugae eggs were present. L. argenticollis and L. atrifacies were reared on A. tsugae in the laboratory, and host records show them to feed exclusively on Adelgidae.     

Fitness and physiology of Adelges tsugae (Hemiptera: Adelgidae) in relation to the health of the eastern hemlock

The hemlock woolly adelgid, Adelges tsugae Annand is an invasive insect that frequently causes hemlock (Tsuga spp.) mortality in the eastern United States. Studies have shown that once healthy hemlocks become infested by the adelgid, nutrients are depleted from the tree, leading to both tree decline and a reduction of the adelgid population. Since A. tsugae is dependent on hemlock for nutrients, feeding on trees in poor health may affect the ability of the insect to obtain necessary nutrients and may consequently affect their physiological and population health. Trees were categorized as lightly or moderately impacted by A. tsugae based on quantitative and qualitative tree health measurements. Population health of A. tsugae on each tree was determined by measuring insect density and peak mean fecundity; A. tsugae physiological health was determined by measuring insect biomass, total carbon, carbohydrate, total nitrogen, and amino nitrogen levels. Adelges tsugae from moderately impacted trees exhibited significantly greater fecundity than from lightly impacted trees. However, A. tsugae from lightly impacted hemlocks contained significantly greater levels of carbohydrates, total nitrogen, and amino nitrogen. While the results of the physiological analysis generally support our hypothesis that A. tsugae on lightly impacted trees are healthier than those on moderately impacted trees, this was not reflected in the population health measurements. Adelges tsugae egg health in response to tree health should be verified. This study provides the first examination of A. tsugae physiological health in relation to standard A. tsugae population health measures on hemlocks of different health levels.     

Implications of early production in an invasive forest pest

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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.     

Short‐term influence of partial cutting on hemlock looper (Lepidoptera: Geometridae) parasitism

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