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

相似文献   

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.     

Failure under stress: the effect of the exotic herbivore Adelges tsugae on biomechanics of Tsuga canadensis

Background and Aims

Exotic herbivores that lack a coevolutionary history with their host plants can benefit from poorly adapted host defences, potentially leading to rapid population growth of the herbivore and severe damage to its plant hosts. The hemlock woolly adelgid (Adelges tsugae) is an exotic hemipteran that feeds on the long-lived conifer eastern hemlock (Tsuga canadensis), causing rapid mortality of infested trees. While the mechanism of this mortality is unknown, evidence indicates that A. tsugae feeding causes a hypersensitive response and alters wood anatomy. This study investigated the effect of A. tsugae feeding on biomechanical properties at different spatial scales: needles, twigs and branches.

Methods

Uninfested and A. tsugae-infested samples were collected from a common garden experiment as well as from naturally infested urban and rural field sites. Tension and flexure mechanical tests were used to quantify biomechanical properties of the different tissues. In tissues that showed a significant effect of herbivory, the potential contributions of lignin and tissue density on the results were quantified.

Key Results Adelges tsugae

infestation decreased the abscission strength, but not flexibility, of needles. A. tsugae feeding also decreased mechanical strength and flexibility in currently attacked twigs, but this effect disappeared in older, previously attacked branches. Lignin and twig tissue density contributed to differences in mechanical strength but were not affected by insect treatment.

Conclusions

Decreased strength and flexibility in twigs, along with decreased needle strength, suggest that infested trees experience resource stress. Altered growth patterns and cell wall chemistry probably contribute to these mechanical effects. Consistent site effects emphasize the role of environmental variation in mechanical traits. The mechanical changes measured here may increase susceptibility to abiotic physical stressors in hemlocks colonized by A. tsugae. Thus, the interaction between herbivore and physical stresses is probably accelerating the decline of eastern hemlock, as HWA continues to expand its range.     

Tree responses to an invasive sap-feeding insect

Although sap-feeding insects are known to negatively affect plant growth and physiology, less is known about sap-feeding insects on woody plants. Adelges tsugae (Annand Hemiptera: Adelgidae), the hemlock woolly adelgid, is an invasive sap-feeding insect in eastern North America that feeds on and kills Tsuga canadensis (L. Carrière), eastern hemlock. Newly hatched adelgid nymphs crawl to young unattacked tissue, settle and immediately enter diapause (aestivation) while attached to hemlock in summer. We assessed the effect of A. tsugae infestation on T. canadensis growth and physiology by analyzing hemlock growth on lateral and terminal branches, water potential, photosynthesis, stomatal conductance, and foliar nitrogen (%N). A. tsugae infestation greatly decreased terminal and lateral growth of eastern hemlock. In addition, A. tsugae presence reduced photosynthesis by 10 % in September and 36 % in October. Adelgid-infested hemlocks also exhibited signs of water stress that included notable reductions in water potential and stomatal conductance. These responses shed light on possible mechanisms of adelgid-induced mortality.     

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.

     

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.     

Range expansion and population dynamics of co-occurring invasive herbivores

Although a range of studies have suggested that competition plays a critical role in determining herbivore assemblages, there has been little work addressing the nature of interactions between competing invasive herbivores. We report the results of research on the hemlock woolly adelgid Adelges tsugae (‘HWA’) and elongate hemlock scale Fiorinia externa (‘EHS’), invasive herbivores that both feed on eastern hemlock (Tsuga canadensis). HWA has been linked to hemlock mortality throughout the East Coast of the US; the loss of hemlock threatens to permanently alter surrounding ecosystems. We assessed the spread and impact of both species by resurveying 142 hemlock stands across a 7,500 km² latitudinal transect, running from coastal CT to northern MA, for HWA and EHS density as well as hemlock mortality. These stands had been previously surveyed in either 1997–1998 (CT) or 2002–2004 (MA). While the number of HWA-infested stands has increased, per-stand HWA density has substantially decreased. In contrast, EHS distribution and density has increased dramatically since 1997–1998. Hemlock mortality was much more strongly related to HWA density than to EHS density, and many stands remain relatively healthy despite an overall increase in hemlock mortality. There was a positive correlation between HWA and EHS densities in stands with low mean HWA densities, suggesting the potential for host-plant-mediated facilitation of EHS by HWA. Our findings underline the importance of research explicitly addressing interactions between competing invasive species, and of determining the potential consequences of these interactions for the invaded ecosystem.     

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.     

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.     

Effect of an exotic herbivore,Adelges tsugae,on photosynthesis of a highly susceptible Tsuga host,with notes on conspecifics

Hemlocks are significant components of temperate forests of Asia and North America, and in eastern North America, they are threatened by an exotic herbivore, the hemlock woolly adelgid, Adelges tsugae. The adelgid is native to Asia and northwestern North America, but is highly invasive in eastern North America where natural enemies are unable to regulate populations and eastern hemlock, Tsuga canadensis, is highly susceptible. In order to gain a better understanding of the metabolic effects of A. tsugae on eastern hemlock, we evaluated its effects on photosynthesis and also evaluated photosynthesis on Tsuga species from various geographic origins. We measured light-saturated photosynthesis (A _sat) and dark respiration of T. canadensis that were infested with adelgid and found a significant decrease in A _sat and a small but significant increase in dark respiration, suggesting that A. tsugae triggers a physiological response in eastern hemlock by decreasing metabolic activity. In a separate experiment, we also measured A _sat of five different hemlock species, including eastern hemlock, the Pacific Northwestern T. heterophylla and T. mertensiana, and the Asian T. diversifolia and T. chinensis. Only weakly significant differences in A _sat were found, with the highest rate in the eastern North American T. canadensis and the lowest in the Pacific Northwestern T. mertensiana. The relatively high photosynthetic rate of T. canadensis could possibly play a role in its susceptibility to A. tsugae. A better understanding of this metabolic response could help develop effective management strategies for combating the highly invasive A. tsugae.     

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.     

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.     

Implications of early production in an invasive forest pest

相似文献   

Widespread inbreeding and unexpected geographic patterns of genetic variation in eastern hemlock (Tsuga canadensis), an imperiled North American conifer

Eastern hemlock (Tsuga canadensis [L.] Carr.) is an ecologically important tree species experiencing severe mortality across much of its eastern North American distribution, caused by infestation of the exotic hemlock woolly adelgid (Adelges tsugae Annand). To guide gene conservation strategies for this imperiled conifer, we conducted a range-wide genetic variation study for eastern hemlock, amplifying 13 highly polymorphic nuclear microsatellite loci in 1,180 trees across 60 populations. The results demonstrate that eastern hemlock exhibits moderate inbreeding, possibly a signature of a prehistoric decline associated with a widespread insect outbreak. Contrary to expectations, populations in formerly glaciated regions are not less genetically diverse than in the putative southern refugial region. As expected, peripheral disjunct populations are less genetically diverse than main-range populations, but some are highly genetically differentiated or contain unique alleles. Spatially explicit Bayesian clustering analyses suggest that three or four Pleistocene glacial refuges may have existed in the Southeastern United States, with a main post-glacial movement into the Northeast and the Great Lakes region. Efforts to conserve eastern hemlock genetic material should emphasize the capture of broad adaptability that occurs across the geographic range of the species, as well as genetic variability within regions with the highest allelic richness and heterozygosity, such as the Southern Appalachians and New England, and within disjunct populations that are genetically distinct. Much genetic variation exists in areas both infested and uninfested by the adelgid.     

Forest dynamics following eastern hemlock mortality in the southern Appalachians

Understanding changes in community composition caused by invasive species is critical for predicting effects on ecosystem function, particularly when the invasive threatens a foundation species. Here we focus on dynamics of forest structure, composition and microclimate, and how these interact in southern Appalachian riparian forests following invasion by hemlock woolly adelgid, HWA, Adelges tsugae. We measured and quantified changes in microclimate; canopy mortality; canopy and shrub growth; understory species composition; and the cover and diversity in riparian forests dominated by eastern hemlock Tsuga canadensis over a period of seven years. Treatments manipulated hemlock mortality either through invasion (HWA infested stands) or girdling (GDL) hemlock trees. Mortality was rapid, with 50% hemlock tree mortality occurring after six years of invasion, in contrast to more than 50% mortality in two years following girdling. Although 50% of hemlock trees were still alive five years after infestation, leaf area lost was similar to that of girdled trees. As such, overall responses over time (changes in light transmittance, growth, soil moisture) were identical to girdled stands with 100% mortality. Our results showed different growth responses of the canopy species, shrubs and ground layer, with the latter being substantially influenced by presence of the evergreen shrub, rhododendron Rhododendron maximum. Although ground layer richness in the infested and girdled stands increased by threefold, they did not approach levels recorded in hardwood forests without rhododendron. Increased growth of co‐occurring canopy trees occurred in the first few years following hemlock decline, with similar responses in both treatments. In contrast, growth of rhododendron continued to increase over time. By the end of the study it had a 2.6‐fold higher growth rate than expected, likely taking advantage of increased light available during leaf‐off periods of the deciduous species. Increased growth and dominance of rhododendron may be a major determinant of future responses in southern Appalachian ecosystems; however, our results suggest hemlock will be replaced by a mix of Acer, Betula, Fagus and Quercus canopy genera where establishment is not limited by rhododendron.     

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.     

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”.     

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.     

When one is not necessarily a lonely number: initial colonization dynamics of Adelges tsugae on eastern hemlock, Tsuga canadensis

The ability to establish successfully in a new area can vary considerably among species. In addition to the well-recognized importance of propagule pressure in driving the rates of establishment of biological invaders, the life history strategy of a species can also affect establishment success, such as in the extent to which Allee effects (positive density-dependence), and environmental and demographic stochasticity manifest themselves. We quantified the establishment success of Adelges tsugae, a non-native insect currently invading North American hemlock. We inoculated eastern hemlock host trees with varying densities of this parthenogenetic insect, from 1 to >500 progrediens ovisacs. The number of settled sistens (the subsequent generation) was positively related to the initial density. More interesting, however, was that we recorded successful establishment from released progrediens ovisacs, and the subsequent initiation of the next generation (sistens), in ≈39 % of host trees inoculated with 1 ovisac. The observation that successful establishment can be accomplished by a single ovisac produced by a single individual has important implications in the invasion dynamics and management of A. tsugae.     

Fungi associated with a natural epizootic in Fiorinia externa Ferris (Hemiptera: Diaspididae) populations

Stands of eastern hemlock [(Tsuga canadensis (L.) Carrière] in the northeastern United States are in decline, in part from the attack of elongate hemlock scale, Fiorinia externa Ferris (Hemiptera: Diaspididae). From 2001 to the present, a natural epizootic has been observed in populations of F. externa. Initially discovered at the Mianus River Gorge Preserve in Bedford, New York, the epizootic has also been detected in Pennsylvania, New Jersey and Connecticut. Understanding and assessing the identity of the pathogenic micro‐organisms responsible for this natural mortality is crucial for developing biological controls for this pest. We have isolated and taxonomically and genetically identified entomopathogens, phytopathogens and endophytic fungi associated with F. externa. Isolates of the following were obtained: Colletotrichum sp., Lecanicillium lecanii, Beauveria bassiana, Metarhiziopsis microspora, Myriangium sp., Mycosphaerella sp. anamorph, Nectria sp., Botrytis sp., Phialophora sp. and Fusarium sp.