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Spring bird migration as a dispersal mechanism for the hemlock woolly adelgid

DOI:10.1007/s10530-019-01918-w
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Nicholas J. Russo at University of California, Los Angeles
Nicholas J. Russo
Chris S. Elphick
Chris S. Elphick
Chris S. Elphick
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Nathan P Havill at US Forest Service
Nathan P Havill
Morgan W. Tingley
Morgan W. Tingley
Morgan W. Tingley
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Abstract and Figures

In eastern North America, the invasive hemlock woolly adelgid (Adelges tsugae Annand), has expanded northward at a pace that exceeds predictions from mechanistic models, suggesting successful long-distance dispersal despite the only viable dispersive phase being a flightless nymph, or “crawler.” We hypothesize that migrating birds may contribute to long-distance dispersal of crawlers by passively transporting them in their plumage during northward migration. We collected hemlock woolly adelgid crawlers from the plumage of wild birds in Connecticut hemlock forests in spring and summer 2016–2017 and evaluated the factors that influence crawler loads on wild birds. Of 456 birds examined, 40 individuals of 22 species carried adelgid crawlers. Crawler loads varied strongly over time, showing a mid-spring peak that mirrored the phenological pattern in crawler abundance. However, crawler load was not affected by either local crawler abundance at capture sites or the degree of bird species association with hemlock forests. To test whether dispersed crawlers could start new invasions, we experimentally simulated avian-assisted dispersal of adelgids onto uninfested nursery hemlocks. Although rare, crawlers placed on birds did settle successfully on experimental branches during the adelgid’s summer generation. Our study confirms that birds carry hemlock woolly adelgid crawlers most often during the period of peak spring songbird migration, and that crawlers can move off bird plumage to settle on hemlock foliage. Bird-mediated, long-distance dispersal of crawlers likely has played a key role in hemlock woolly adelgid spread, and with warming temperatures, this mechanism may continue to be important for future range expansion.
Range of eastern hemlock and invasive hemlock woolly adelgid in eastern North America relative to sampling sites. Hemlock woolly adelgid was first detected in eastern North America in 1951 and has since spread throughout much of the range of the eastern hemlock—particularly northward and eastward. In 2016 and 2017, we sampled for adelgids on wild birds caught at five sites in Connecticut, USA (inset; black outline on large map), where hemlock woolly adelgid first appeared in the 1980s. Map data on hemlock and adelgid range courtesy of USDA Forest Service, Northeastern Area State and Private Forestry, Forest Health Protection
Range of eastern hemlock and invasive hemlock woolly adelgid in eastern North America relative to sampling sites. Hemlock woolly adelgid was first detected in eastern North America in 1951 and has since spread throughout much of the range of the eastern hemlock—particularly northward and eastward. In 2016 and 2017, we sampled for adelgids on wild birds caught at five sites in Connecticut, USA (inset; black outline on large map), where hemlock woolly adelgid first appeared in the 1980s. Map data on hemlock and adelgid range courtesy of USDA Forest Service, Northeastern Area State and Private Forestry, Forest Health Protection
… 
Schematic showing phenology of hemlock woolly adelgid life cycle and bird migration in eastern North America. The hemlock woolly adelgid has two generations per year, each with four instars, with mobile crawlers hatching in spring and summer. Birds have the potential to pick up dispersing crawlers whenever crawlers are present and active, but the greatest potential for long-distance dispersal occurs with the synchrony of the spring generation of crawlers with northward migrating birds. Adelgid crawlers and life stages are not drawn to scale. Graphic created by Vincent D’Amico (USDA Forest Service)
Schematic showing phenology of hemlock woolly adelgid life cycle and bird migration in eastern North America. The hemlock woolly adelgid has two generations per year, each with four instars, with mobile crawlers hatching in spring and summer. Birds have the potential to pick up dispersing crawlers whenever crawlers are present and active, but the greatest potential for long-distance dispersal occurs with the synchrony of the spring generation of crawlers with northward migrating birds. Adelgid crawlers and life stages are not drawn to scale. Graphic created by Vincent D’Amico (USDA Forest Service)
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Phenological trends in hemlock woolly adelgid across 5 hemlock forests in Connecticut. a Temporal variation in ambient crawler abundance on hemlock trees. Points correspond to the standardized number of crawlers per trap per week for each monitored location. A quasi-Poisson generalized linear model was fit to the data, using a flexible quintic polynomial as the functional form for the relationship to day of year. b Number of crawlers collected from birds in hemlock forests in relation to sampling date. The shaded area indicates the 95% confidence interval and mean (solid line) of the relationship to day of year, estimated using the top generalized additive model from the model set (Table 2). Darker-shaded points indicate a higher frequency of the crawler load count
Phenological trends in hemlock woolly adelgid across 5 hemlock forests in Connecticut. a Temporal variation in ambient crawler abundance on hemlock trees. Points correspond to the standardized number of crawlers per trap per week for each monitored location. A quasi-Poisson generalized linear model was fit to the data, using a flexible quintic polynomial as the functional form for the relationship to day of year. b Number of crawlers collected from birds in hemlock forests in relation to sampling date. The shaded area indicates the 95% confidence interval and mean (solid line) of the relationship to day of year, estimated using the top generalized additive model from the model set (Table 2). Darker-shaded points indicate a higher frequency of the crawler load count
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Boxplots summarizing counts of settled summer-generation crawlers based on experiments where 15 crawlers were experimentally tested for their ability to settle on uninfested hemlock branches after 2–4 weeks. Experiments include two negative controls (control 1: a bird perched with no crawlers, n = 10; control 2: no bird perched and no crawlers applied, n = 10), tests where taxidermied birds with crawlers were perched on a branch for either 1 or 15 min (n = 25 each), and direct placement of crawlers onto branches (n = 25). Counts of settled crawlers with different letters indicate comparisons that are significantly different (Fisher’s exact test, p < 0.05). Results of experiments with the spring generation are not shown because experiments only resulted in two successful settlements (see “Discussion”)
Boxplots summarizing counts of settled summer-generation crawlers based on experiments where 15 crawlers were experimentally tested for their ability to settle on uninfested hemlock branches after 2–4 weeks. Experiments include two negative controls (control 1: a bird perched with no crawlers, n = 10; control 2: no bird perched and no crawlers applied, n = 10), tests where taxidermied birds with crawlers were perched on a branch for either 1 or 15 min (n = 25 each), and direct placement of crawlers onto branches (n = 25). Counts of settled crawlers with different letters indicate comparisons that are significantly different (Fisher’s exact test, p < 0.05). Results of experiments with the spring generation are not shown because experiments only resulted in two successful settlements (see “Discussion”)
… 
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ORIGINAL PAPER
Spring bird migration as a dispersal mechanism
for the hemlock woolly adelgid
Nicholas J. Russo .Chris S. Elphick .Nathan P. Havill .Morgan W. Tingley
Received: 5 July 2018 / Accepted: 14 January 2019 / Published online: 23 January 2019
©Springer Nature Switzerland AG 2019
Abstract In eastern North America, the invasive
hemlock woolly adelgid (Adelges tsugae Annand),
has expanded northward at a pace that exceeds
predictions from mechanistic models, suggesting
successful long-distance dispersal despite the only
viable dispersive phase being a flightless nymph, or
“crawler.” We hypothesize that migrating birds may
contribute to long-distance dispersal of crawlers by
passively transporting them in their plumage during
northward migration. We collected hemlock woolly
adelgid crawlers from the plumage of wild birds in
Connecticut hemlock forests in spring and summer
2016–2017 and evaluated the factors that influence
crawler loads on wild birds. Of 456 birds examined,
40 individuals of 22 species carried adelgid crawlers.
Crawler loads varied strongly over time, showing a
mid-spring peak that mirrored the phenological
pattern in crawler abundance. However, crawler load
was not affected by either local crawler abundance at
capture sites or the degree of bird species association
with hemlock forests. To test whether dispersed
crawlers could start new invasions, we
experimentally simulated avian-assisted dispersal of
adelgids onto uninfested nursery hemlocks. Although
rare, crawlers placed on birds did settle successfully
on experimental branches during the adelgid’s sum-
mer generation. Our study confirms that birds carry
hemlock woolly adelgid crawlers most often during
the period of peak spring songbird migration, and that
crawlers can move off bird plumage to settle on
hemlock foliage. Bird-mediated, long-distance dis-
persal of crawlers likely has played a key role in
hemlock woolly adelgid spread, and with warming
temperatures, this mechanism may continue to be
important for future range expansion.
Keywords Adelges tsugae · Biotic interactions ·
Phenology · Invasive species · Ectozoochory
Introduction
Birds contribute to the exchange of organisms among
ecosystems by carrying plant and animal propagules
on their bodies or in their digestive tracts during
migration (Viana et al. 2013; Bauer and Hoye 2014).
Numerous studies of species with disjunct ranges
implicate migratory birds as dispersal vectors, espe-
cially in cases where species divergence times are
anachronous with potentially explanatory geological
events (Stevens and Hogg 2003; Popp et al. 2011;
Lewis et al. 2014; Havill et al. 2016). Birds transport
other organisms via two processes: endozoochory, or
N. J. Russo · C. S. Elphick · M. W. Tingley (&)
Department of Ecology and Evolutionary Biology,
University of Connecticut, 75 N. Eagleville Rd., Unit
3043, Storrs, CT 06269-3043, USA
e-mail: morgan.tingley@uconn.edu
N. P. Havill
Northern Research Station, United States Forest Service,
Hamden, CT 06514, USA
123
Biol Invasions (2019) 21:1585–1599
https://doi.org/10.1007/s10530-019-01918-w(0123456789().,-volV)(0123456789().,-volV)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... We also included locations invaded by HWA in the USA that were within 70 km of the Canadian border. Long-distance HWA spread is assisted by migratory birds (Russo et al., 2019), so we used data from Ewert et al. (2012) and Birds Canada (2019) to identify key migration corridors across southern Ontario. The migratory pathways of birds likely to carry HWA (Russo et al., 2019) follow the shorelines of the Great Lakes, so we assumed that the spread paths did not cross Lakes Erie and Ontario. ...
... Long-distance HWA spread is assisted by migratory birds (Russo et al., 2019), so we used data from Ewert et al. (2012) and Birds Canada (2019) to identify key migration corridors across southern Ontario. The migratory pathways of birds likely to carry HWA (Russo et al., 2019) follow the shorelines of the Great Lakes, so we assumed that the spread paths did not cross Lakes Erie and Ontario. Thus, to calculate the dispersal distances between pairs of uninvaded sites and the nearest invaded site, we used the shortest path algorithm (Dijkstra, 1959) traced over land locations and excluded long-distance dispersal over these two lakes. ...
Hierarchical governance in invasive species survey campaigns
Article
Large-scale delimiting surveys are critical for detecting pest invasions and often undertaken at different governance levels. In this study, we consider two-level hierarchical planning of surveys of harmful invasive pests including a government agency with a mandate to report the spatial extent of an invasion, and regional governments (counties) concerned about the possible threat of an outbreak. The central agency plans delimiting pest surveys across multiple administrative subdivisions. Counties could participate in these surveys if funds become available. Our goal is to find the optimal levels of cooperation between the central agency and regional governments in the form of the central agency sharing funds with regional governments in a way that benefits both it and the other entities. We propose a Stackelberg game model that finds optimal levels of collaboration between two levels of government in large-scale pest survey campaigns. We apply the model to surveillance of hemlock woolly adelgid, a harmful pest of hemlock trees in Ontario, Canada. Our solutions help anticipate the underperformance of surveys conducted by regional governments because their goals do not fully align with the central agency survey objective. The methodology can be adapted to explore governance hierarchies in other regions and political jurisdictions.
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... The perturbation of normal migratory patterns also likely has wider-ranging ecological ramifications. Avian migrants are responsible for the widespread and rapid dispersal of parasites, pathogens, and propagules-linking distinct ecosystems across wide geographical areas 7,8,[66][67][68] . With the speed and probability of range expansions heavily impacted by rare, long-distance dispersal events 1 , vagrant birds transporting organisms far beyond their expected range have an outsized impact on the range expansion of these populations 8 . ...
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Rare birds known as “accidentals” or “vagrants” have long captivated birdwatchers and puzzled biologists, but the drivers of these rare occurrences remain elusive. Errors in orientation or navigation are considered one potential driver: migratory birds use the Earth’s magnetic field—sensed using specialized magnetoreceptor structures—to traverse long distances over often unfamiliar terrain. Disruption to these magnetoreceptors or to the magnetic field itself could potentially cause errors leading to vagrancy. Using data from 2 million captures of 152 landbird species in North America over 60 years, we demonstrate a strong association between disruption to the Earth’s magnetic field and avian vagrancy during fall migration. Furthermore, we find that increased solar activity—a disruptor of the avian magnetoreceptor—generally counteracts this effect, potentially mitigating misorientation by disabling the ability for birds to use the magnetic field to orient. Our results link a hypothesized cause of misorientation to the phenomenon of avian vagrancy, further demonstrating the importance of magnetoreception among the orientation mechanisms of migratory birds. Geomagnetic disturbance may have important downstream ecological consequences, as vagrants may experience increased mortality rates or facilitate range expansions of avian populations and the organisms they disperse.
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... Magsig-Castillo et al. (2010) showed that under laboratory conditions some Diaspididae species were also able to attach to other insect species to be carried for short distances, with some individuals remaining attached to their carrier after one hour. There is also recent evidence for a North American invasive species, Adelges tsugae (hemlock wooly adelgid), that foraging birds may serve as a vector for long-distance movement of crawlers (Russo et al., 2019). However, such experiments have not been conducted for C. pinifoliae. ...
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... Crawlers of the hemlock woolly adelgid Adelges tsugae Annand (Hemiptera: Adelgidae) actively attach to birds during the spring migration and thus ensure dispersal (Russo et al. 2016). In eastern North America, this dispersal of crawlers by a variety of migratory birds has resulted in the woolly adelgid becoming a major invasive threat in hemlock forests (Russo et al. 2019). The settling of crawlers onto hemlock branches where they will metamorphose into sedentary nymphs is directly affected by the visible spectrum of sunlight and not by ultraviolet radiation; crawlers appear to be negatively phototactic and/or thermotactic (Mayfield and Jetton 2020). ...
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The ability to disperse is vital for all organisms, but especially for those whose habitats deteriorate, necessitating relocation to better feeding or breeding sites. Phoresy is assisted dispersal in which one organism uses another as its vehicle. In this review, phoresy will be largely restricted to cases wherein the rider is not parasitic on the vehicular stage used for dispersal, and in which insects are riders or rides. Phoresy occurs in organisms with limited mobility, and in secondarily brachypterous or completely wingless insects. Intraspecific phoresy also occurs. Generally, immature stages resistant to environmental assaults, such as dauers in nematodes, triungulins in beetles, or deutonymphs in mites, undertake phoresy. A size differential between rider and rider enables several conspecifics to board the same vehicle, likely ensuring mating opportunities at the destination. Riders may have special attachment devices or adhesive secretions to ensure safety during travel. Life cycles of riders and vehicles are often synchronized, and when phoresy is mutualistic, vehicles may also employ chemical tactics to achieve this synchrony. Chemical cues help to identify the appropriate vehicle, for disembarkation, or to lure the vehicle towards riders. Most riders prefer female vehicles, possibly to ensure access to rich nesting sites. Density-dependent selection may operate to limit the number of riders on a vehicle and phoresy may also facilitate sexual selection among riders. Whether vehicles can avoid phoresy is barely understood. This review attempts to place phoresy within a broad evolutionary context and points out the paucity of knowledge in certain research areas.
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... Just like the spread of A. tsugae themselves, their eDNA can be transported over long distances via birds and other insect vectors (Russo et al., 2016;Russo et al., 2019). Further studies exploring the persistence of eDNA associated with foliage surfaces and A. tsugae wool will enhance the interpretation of positive eDNA detections, and aid in developing strategies to use visual inspection complimentary with eDNA surveillance. ...
Sensitive environmental DNA (eDNA) methods to detect hemlock woolly adelgid and its biological control predators Leucotaraxis silver flies and a Laricobius beetle
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Full-text available
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Environmental DNA (eDNA) analysis can be a powerful tool for the early detection of invasive organisms. However, research on terrestrial eDNA detection from foliage surfaces has been limited. In this study, we developed methods to capture and detect eDNA using qPCR from an invasive forest pest, hemlock woolly adelgid (Adelges tsugae), and three of its biological control predators Leucotaraxis piniperda, Leucotaraxis argenticollis, and Laricobius nigrinus. We designed four highly efficient qPCR assays with a low limit of detection (1–10 copies/reaction). The assay targeting A. tsugae was species-specific. The assays targeting Le. piniperda, and Le. argenticollis were biotype-specific in addition to being species-specific demonstrating applications of eDNA analysis beyond species-level detection. The La. nigrinus assay also detected DNA from closely related and hybridizing Laricobius rubidus. The eDNA methods were evaluated against traditional detection methods. We collected foliage samples from three strata (bottom, middle, and top) of eastern hemlock trees to detect the presence of A. tsugae. The detection of the biological control predators was evaluated using western hemlock foliage samples collected from the predators' native range in western Washington. The eDNA methods had significantly higher positive detection rates (2.8–4.5 times) than conventional methods of all target species. The strata of sampling were not significant in determining the presence of A. tsugae infestation. The eDNA concentration positively correlated with the observed density for all species. This study demonstrates the efficacy of eDNA analysis as a more sensitive tool for early detection of A. tsugae and to track the establishment of its biological control predators. © 2022 The Authors. Environmental DNA published by John Wiley & Sons Ltd.
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... However, the potential implications of birds as dispersal vectors in various groups (including vascular plant seeds, fern and bryophyte spores and fragments, and propagules of lichenized and nonlichenized fungi, algae, and microorganisms) are vast (Viana et al., 2016). These range from explaining biogeographical patterns (Biersma et al., 2017;Garrido-Benavent & Perez-Ortega, 2017;Lovas-Kiss et al., 2019) to distribution dynamics of invasive species (Lovas-Kiss et al., 2019;Molefe et al., 2020;Russo et al., 2019) and the spread of pathogens (Alfonzo et al., 2013;Hubálek, 2004), both in terrestrial and in aquatic ecosystems (Coughlan et al., 2017;Hessen et al., 2019). In fragmented landscapes, understanding the role of dispersal and connectivity in conservation is important (Keeley et al., 2018;Trakhtenbrot et al., 2005), but due to a general lack of information, modeling approaches and connectivity measures rarely take into account the potential of animal-mediated dispersal (Rogers et al., 2019;Viana et al., 2016). ...
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Bird‐mediated dispersal is presumed to be important in the dissemination of many different types of organisms, but concrete evidence remains scarce. This is especially true for biota producing microscopic propagules. Tree‐dwelling birds, such as woodpeckers, would seem to represent ideal dispersal vectors for organisms growing on standing tree trunks such as epiphytic lichens and fungi. Here, we utilize bird natural history collections as a novel source of data for studying dispersal ecology of plants, fungi, and microorganisms. We screened freshly preserved specimens of three Finnish woodpecker species for microscopic propagules. Samples were taken from bird feet, and chest and tail feathers. Propagules were extracted using a sonication–centrifugation protocol, and the material obtained was studied using light microscopy. Diverse biological material was recovered from all specimens of all bird species, from all positions sampled. Most abundant categories of discovered biological material included bryophyte fragments, fungal spores, and vegetative propagules of lichens. Also, freshwater diatoms, bryophyte spores, algal cells, testate amebae, rotifers, nematodes, pollen, and insect scales were identified. The method developed here is applicable to living specimens as well, making it a versatile tool for further research. Our findings highlight the potential of bird‐mediated dispersal for diverse organisms and showcase the use of natural history collections in ecological research.
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... Information on the proximity of hemlock stands to existing HWA infestations, along with the presence of dispersal corridors such as trails, roads, riparian corridors (Koch et al., 2006), and railroads (Liang et al., 2014) may act as additional factors in HWA spread. Finally, incorporation of bird migratory routes may lend to increased predictive power given the ability of HWA to attach to and disperse via birds over long distances (Russo et al., 2019), and the identification of stands with high social and economic value can inform the prioritization of monitoring efforts. ...
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The invasive hemlock woolly adelgid (HWA) has decimated hemlock stands across much of the eastern United States, and presents a significant threat to all eastern hemlock in Canada across Ontario, Quebec, New Brunswick, Nova Scotia, and Prince Edward Island, especially since the recent detection of its widespread establishment in southwest Nova Scotia. The spread and rising infestation level and impacts of HWA in this region serve as a warning for forest managers across eastern Canada to develop appropriate management plans and priorities. The HWA decision framework presented here aims to prepare forest managers in eastern Canada for the decisions and challenges that they will face, from prevention, detection, and control, to hemlock ecosystem restoration and management program evaluation. We review the strategies and tactics that are currently available, that are being developed, and that show the most promise to date. Given the nature of HWA, the long-term outlook for eastern hemlock in Canada will likely feature HWA as a component of hemlock ecosystems across much of the region, necessitating a comprehensive, adaptive management program to mitigate its ecosystem consequences. (https://www.sciencedirect.com/science/article/pii/S0378112719302920)
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Differential sunlight exposure affects settling behaviour of hemlock woolly adelgid crawlers
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• Previous research demonstrated that elevated sunlight improves carbon balance and growth of eastern hemlock (Tsuga canadensis (L.) Carrière) seedlings infested with the invasive hemlock woolly adelgid (Adelges tsugae Annand). • This study examined the hypothesis that elevated visible and ultraviolet sunlight directly affects the settling behaviour of A. tsugae crawlers. • Hemlock seedlings were manually infested with equal densities of A. tsugae and placed into artificial shade treatments (0%, 40% and 80% shade). The density of settled nymphs of the ensuing generation on shaded seedlings was three times higher than the density on unshaded seedlings. • Adelges tsugae ovisacs were also attached to hydrated hemlock branches placed beneath acrylic filter treatments that selectively allowed transmission of various sunlight wavelengths. The proportion of adelgid crawlers that settled on the branch (vs. dropping from it) was higher beneath filters that blocked the widest spectrum of solar radiation (opaque and amber filters) than beneath full sun. In the March‐April trial, exposure to full sun and the full visible spectrum only (clear‐UV filter) significantly increased the proportion of crawlers that settled on the bottom (vs. top) side of the branch. • Our results suggest that A. tsugae crawlers are negatively phototactic and/or thermotactic, with behaviour influenced more by visible light than ultraviolet light.
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Hemlock Woolly Adelgid Management Plan for Canada
Technical Report
Full-text available
  • Jun 2018
The hemlock woolly adelgid (HWA) is an aphid-like invasive pest from Asia that threatens hemlock survival in the eastern United States and more recently in eastern Canada. Hemlock is an important tree species because it is slow-growing and long-lived, with large canopies that create unique habitat that many plants and animals rely on. Hemlock are also very important to recreationalist and homeowners who enjoy and admire the unique environment that hemlock provide. The aim of this report is to outline the components for a HWA management plan in all eastern provinces that have hemlock at risk to HWA (i.e. Ontario, Quebec, New Brunswick, Nova Scotia, and Prince Edward Island). First, we summarize the risks and potential impacts associated with HWA in eastern Canada. We then outline potential components of an HWA management plan in Canada by summarizing the research and management tactics already explored and implemented in the eastern United States.
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Mortality and Recovery of Hemlock Woolly Adelgid (Adelges tsugae) in Response to Winter Temperatures and Predictions for the Future
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Full-text available
  • Dec 2017
Eastern (Tsuga canadensis) and Carolina hemlocks (T. caroliniana) of eastern North America have been attacked by the non-native hemlock woolly adelgid (Adelges tsugae Annand) (HWA) since the first half of the 20th century. Unlike most insects, HWA develops through one generation from fall to late winter, exposing this insect to the lethal effects of winter temperatures. The mortality inflicted by winter temperatures on HWA determines the surviving population density as well as its ability to spread to uninfested areas. With the ongoing changes in climate, knowledge of this species’ ability to survive and spread in the future can help land managers prepare for its management. This study began during the winter of 2014 and ended in the spring of 2017. During this period, winter mortality of HWA was recorded at 100 sites from Maine to Georgia (n = 209). Changes in population density from the sistens to the succeeding progrediens generation were recorded at 24 sites (n = 35). Models were developed to predict HWA mortality using the lowest minimum temperature prior to the mortality assessment date, the number of days with mean temperature <−1 °C, and the mean daily temperature of the three days preceding that minimum. Models were also developed to predict population density changes from the overwintering sistens generation to the following progrediens generation. Future projections under climate change showed increases in winter survival and population growth rates over time. Especially towards the northeastern edge of T. canadensis’ distribution as minimum temperatures are predicted to increase at a greater rate. This will result in an increase in density throughout its current distribution and expansion northward causing an increase in its impact on eastern Tsuga spp.
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Predicting Hemlock Woolly Adelgid Winter Mortality in Connecticut Forests by Climate Divisions
Article
Full-text available
  • Mar 2017
Hemlock Woolly Adelgid (HWA) is a devastating non-native pest of North American Tsuga canadensis (Eastern Hemlock) and Tsuga caroliniana (Carolina Hemlock). I analyzed 15 years of data collected during the period 2000-2015 to determine important winter variables influencing HWA mortality in the 3 Connecticut climatic divisions. Absolute minimum daily winter temperature, the number of subzero days (temperature drops below-17.8 °C [0 °F]), and a new interaction variable-negative degree days (NDD)-were identified as significant predictors of HWA winter mortality. The absolute minimum daily winter temperature was the most critical factor. Minimum daily winter temperatures of-24 °C, 5.5 subzero days, and-130 NDD in Division 1(Northwest);-22.4 °C, 6 subzero days, and-100 NDD in Division 2 (Central); and-21.2 °C, 2.6 subzero days, and-45 NDD in Division 3 (Coastal) resulted in 90% HWA mortality. Patterns of HWA winter mortality in coastal Division 3 were distinct from the interior and suggest cold adaptation in northern interior populations. Recent, consecutive, arctic cold air outbreaks associated with weak polar vortex events have greatly reduced HWA populations statewide, with implications for the survival, spread, and control of HWA in the northeastern US.
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Generalist birds promote tropical forest regeneration and increase plant diversity via rare-biased seed dispersal
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  • Jul 2016
Regenerated forests now compose over half of the world's tropical forest cover and are increasingly important as providers of ecosystem services, freshwater, and biodiversity conservation. Much of the value and functionality of regenerating forests depends on the plant diversity they contain. Tropical forest diversity is strongly shaped by mutualistic interactions between plants and fruit-eating animals (frugivores) that disperse seeds. Here we show how seed dispersal by birds can influence the speed and diversity of early successional forests in Puerto Rico. For two years, we monitored the monthly fruit production of bird-dispersed plants on a fragmented landscape, and measured seed dispersal activity of birds and plant establishment in experimental plots located in deforested areas. Two predominantly omnivorous bird species, the Northern Mockingbird (Mimus polyglottos) and the Gray Kingbird (Tyrannus dominicensis), proved critical for speeding up the establishment of woody plants and increasing the species richness and diversity of the seed rain in deforested areas. Seed dispersal by these generalists increased the odds for rare plant species to disperse and establish in experimental forest-regeneration plots. Results indicate that birds that mix fruit and insects in their diets and actively forage across open and forested habitats can play keystone roles in the regeneration of mutualistic plant-animal communities. Furthermore, our analyses reveal that rare-biased (antiapostatic) frugivory and seed dispersal is the mechanism responsible for increasing plant diversity in the early-regenerating community.
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Migratory Birds as Global Dispersal Vectors
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Propagule dispersal beyond local scales has been considered rare and unpredictable. However, for many plants, invertebrates, and microbes dispersed by birds, long-distance dispersal (LDD) might be regularly achieved when mediated by migratory movements. Because LDD operates over spatial extents spanning hundreds to thousands of kilometers, it can promote rapid range shifts and determine species distributions. We review evidence supporting this widespread LDD service and propose a conceptual framework for estimating LDD by migratory birds. Although further research and validation efforts are still needed, we show that current knowledge can be used to make more realistic estimations of LDD mediated by regular bird migrations, thus refining current predictions of its ecological and evolutionary consequences.
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