Variable colonization by the hemlock woolly adelgid suggests infestation is associated with hemlock host species

Abstract

Studies increasingly indicate host resistance likely influences hemlock woolly adelgid (HWA) populations. We describe coexisting HWA populations in four hemlock species, three from HWA’s native range (Tsuga chinensis, T. dumosa, and T. sieboldii) and one from its introduced range: T. canadensis. HWA populations were greater in T. canadensis and lesser or absent in T. chinensis and T. dumosa. HWA stylet insertion was observed the least in T. chinensis and T. dumosa, suggesting a physical and/or chemical feeding deterrent. While T. chinensis and T. dumosa consistently and distinctly differed from T. canadensis, T. sieboldii grouped with T. canadensis or T. chinensis and T. dumosa in different experiments, suggesting mechanisms influencing HWA populations differ by host species. HWA were found more often on tops of T. chinensis and T. dumosa branches but equally on tops and bottoms of T. canadensis branches, corresponding with locations of trichomes (which T. sieboldii lacks). Evidence from the literature about dissimilarities in hemlock hosts (e.g., HWA interactions and vulnerability, feeding damage response, cuticle thickness, terpenoid chemistry, arthropod and microbial communities) and native and introduced HWA populations (e.g., losses of sexual reproduction and primary spruce host) suggests a limit to applying information from native systems to management in introduced systems.

Graphic abstract

Appendix

Worldwide hemlock species (Farjon 2017; Holman et al. 2017) and associated environmental conditions.

Species	Climate and habitat	References
T. canadensis (L.) Carrière	Grows from sea level to 1520 m in well-drained moist and very moist sandy loams, loamy sands, and silt loams, on hillsides, rocky ridges, and ravines in subtropical and continental humid temperate deciduous (1′) and boreal (2′) forests at mean temperatures of − 12 (January) to 16 °C (July) with annual precipitation < 740 to > 1520 mm	Farjon (1990), Godman and Lancaster (1990), Taylor (1993)
T. caroliniana Engelm	Grows from 600 to 1500 m in ravines and canyons in shallow, nutrient-poor soils in subtropical cool, humid boreal (1′) and temperate deciduous (2′) forests; stress tolerant but dry season intolerant, cold hardy − 17.8 to − 23.2 °C with > 1000 m annual precipitation	Farjon (1990), Godman and Lancaster (1990), Taylor (1993), Humphrey (1989), Bannister and Neuner (2001)
T. chinensis (Franch.) E. Pritz	Grows at 1000 to 3500 m in limestone or granite-derived soils in very wet and cool, monsoon tropical mountain, ridge conifer, closed evergreen tropical, and seasonal coniferous submontane forests, also in valleys and river basins, at annual mean temperatures ranging from 14 to 19 °C and > 2000 mm annual precipitation	Pritzel (1900), Wu and Raven (1999), Nguyen et al. (2000), Bannister and Neuner (2001), Nguyen and Thomas (2004), Nguyen et al. (2004)
T. diversifolia (Maxim.) Mast	Grows at 700 to 2000 m in dry, podzolic soils, sometimes on volcanic or igneous rock, in cool climates with cold, snowy winters and abundant summer rainfall	Numata et al. (1972), Katsuki and Luscombe (2013)
T. dumosa (D. Don) Eichler	Grows at 2000 to 3500 m in granite-derived soils in high-mountain and river basin mixed conifer forest, closed evergreen tropical seasonal mixed subalpine forest, and fire-damaged mixed forest at annual mean temperatures ranging from 13 to 18 °C and 2000 to 3500 mm annual precipitation	Nguyen and Vidal (1996), Vu Van Dung (1996), Wu and Raven (1999), Nguyen et al. (2004)
T. forrestii Downie	Grows at 2000 to 3500 m in temperate to cold temperate mountains, valleys, and mixed forests, often in podzolized soils with 1000 to 2000 mm precipitation	eFloras (2008), Farjon (2017)
T. heterophylla (Raf.) Sarg	Grows from sea level to 2130 m in a variety of well-drained soils, on all bedrock types, and on all major landforms in marine west coast and highland boreal forests at mean annual temperatures ranging from 0.3 to 11.3 °C with annual precipitation of < 380 to > 6650 mm	Packee (1990), Taylor (1993)
T. mertensiana (Bong.) Carrière	Grows from sea level to 2400 m in loose, coarse-grained, well-drained soils, thick organic soils, and decayed wood in mixed stands on sheltered slopes in marine west coast and highland boreal subalpine forests at mean annual temperatures ranging from 3 to 4 °C and annual precipitation from 971 to 3021 mm	Taylor (1993), Means (1990)
T. sieboldii Carrière	Grows in temperate/warm-temperate (sub-Mediterranean) climates in dry, shallow soils, sometimes with exposed bedrock, on steep slopes, ridges, and mountain summits in the transitional zone between evergreen and summergreen broad-leaved forests	Numata et al. (1972)
T. ulleungensis	Grows from 310 to 500 m on north-facing, well-drained rocky ridges in Pinus parviflora dominated forests	Holman et al. (2017)