Abstract
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.
Similar content being viewed by others
References
Adkins JK, Rieske LK (2013) Loss of a foundation forest species due to an exotic invader impacts terrestrial arthropod communities. For Ecol Manag 295:126–135. doi:10.1016/j.foreco.2013.01.012
Bentz SE, Riedel LGH, Pooler MR, Townsend AM (2002) Hybridization and self-compatibility in controlled pollinations of eastern North American and Asian hemlock (Tsuga) species. J Arboric 28:200–205
Broeckling CD, Salom SM (2003) Volatile emissions of eastern hemlock, Tsuga canadensis, and the influence of hemlock woolly adelgid. Phytochemistry 62:175–180
Butin E, Preisser E, Elkinton J (2007) Factors affecting settlement rate of the hemlock woolly adelgid, Adelges tsugae, on eastern hemlock, Tsuga canadensis. Agric. Forest Entomol. 9:215–219
Del Tredici P, Kitajima A (2004) Introduction and cultivation of Chinese hemlock (Tsuga chinensis) and its resistance to hemlock woolly adelgid (Adelges tsugae). J Arboric 30:282–287
Domec JC, Rivera LN, King JS, Peszlen I, Hain F, Smith B, Frampton J (2013) Hemlock woolly adelgid (Adelges tsugae) infestation affects water and carbon relations of eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana). New Phytol 199(2):452–463. doi:10.1111/nph.12263
Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486
Ericsson A, Hellkvist J, Hiller-Hadalgstromer K, Larsson S, Matton-Djos, Tenow O (1980) Consumption and pine growth—hypotheses on effects on growth processes by needle-eating insects. In: Persson T (ed) Structure and function of northern coniferous forests: an ecosystem study. Ecological Bulletins 32:537–545
Farjon A (1990) Pinaceae: Drawings and descriptions of the genera Abies, Cedrus, Pseudolarix, Keteleeria, Nothotsuga, Tsuga, Cathaya, Pseudotsuga, Larix, and Picea, 121st edn. Koeltz Scientific Books, Konigstein
Finzi A, Van Breemen N, Canham CD (1998) Canopy tree-soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–446
Ford CR, Vose JM (2007) Tsuga canadensis (L.) Carr. mortality will impact hydrologic processes in southern Appalachian forest ecosystems. Ecol Appl 17:1156–1167
Glerum C (1980) Food sinks and food reserves of trees in temperate climates. N Z J For Sci 10:176–185
Glerum C, Balatinecz JJ (1980) Formation and distribution of food reserves during autumn and their subsequent utilization in jack pine. Can J Botany 58:40–54
Godman RM, Lancaster K (1990) Tsuga canadensis. In: Burns RM, Honkala BH (eds) Silvics of North America vol 1. Conifers. Agricultural Handbook 654. USDA Forest Service, Washington, DC
Gonda-King L, Radville L, Preisser EL (2012) False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale. Environ Entomol 41:523–531. doi:10.1603/EN11227
Gordon JC, Larson PR (1970) Redistribution of 14C-labeled reserve food in young red pines during shoot elongation. For Sci 16:14–20
Hadley JL (2000) Understory microclimate and photosynthetic response of saplings in an old-growth eastern hemlock (Tsuga canadensis L.) forest. Ecoscience 7:66–72
Havill NP, Montgomery ME, Yu GY, Shiyake S, Caccone A (2006) Mitochondrial DNA from hemlock woolly adelgid (Hemiptera: Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Ann Entomol Soc Am 99:195–203
Hunter JJ, Visser JH (1988) The effect of partial defoliation, leaf position and developmental stage of the vine on the photosynthetic activity of Vitis vinifera L. cv Cabernet Sauvignon. S Afr J Enol Vitic 9:9–15
Ishii H, Kitaoka S, Fujisaki T, Maruyama Y, Koike T (2007) Plasticity of shoot and needle morphology and photosynthesis of two Picea species with different site preferences in northern Japan. Tree Physiol 27:1595–1605
Jenkins JC, Aber JD, Canham CD (1999) Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests. Can J For Res 29:630–645
Jetton RM, Dvorak WS, Whittier WA (2008) Ecological and genetic factors that define the natural distribution of Carolina hemlock in the southeastern United States and their role in ex situ conservation. For Ecol Manag 255:3212–3221
Joseph SV, Braman SK, Hanula JL (2011) Effects of fertilization of four hemlock species on Adelges tsugae (Hemiptera: Adelgidae) growth and feeding preference of predators. J Econ Entomol 104:288–298
Kohler GR, Stiefel VL, Wallin KF, Ross DW (2008) Predators associated with the hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environ Entomol 37:494–504
Lagalante AF, Montgomery ME (2003) Analysis of terpenoids from hemlock (Tsuga) species by solid-phase microextraction/gas chromatography/ion-trap mass spectrometry. J Agric Food Chem 51:2115–2120
Lagalante AF, Lewis N, Montgomery ME, Shields KS (2006) Temporal and spatial variation of terpenoids in eastern hemlock (Tsuga canadensis) in relation to feeding by Adelges tsugae. J Chem Ecol 32:2389–2403
Lemmon JG (1890) Cone-bearers of California. Third biennial report of the California state Board of Forestry for the years 1887–99, to Governor R. W. Waterman. California State Board of Forestry, Sacramento
LI-COR Biosciences Inc (2004) Using the LI-6400/LI-6400XT Portable Photosynthesis System. Lincoln, Nebraska
Mausel DL (2005) Observations on fecundity and natural enemies of hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae) in Seattle, Washington. Pan-Pac Entomol 81:97–98
Mauseth JD (2003) Botany: an introduction to plant biology, 3rd edn. Jones and Barlett Publishers Inc., Sudbury
McClure MS (1991) Density-dependent feedback and population-cycles in Adelges tsugae (Homoptera, Adelgidae) on Tsuga canadensis. Environ Entomol 20:258–264
McClure MS (1992) Hemlock woolly adelgid. Am Nurserym 175:82–89
McClure MS, Salom SM, Shields KS (2001) Hemlock woolly adelgid. USDA Forest Service FHTET-2001-03. Morgantown, WV
Means JE (1990) Mountain hemlock, Tsuga mertensiana (Bong.) Carr. In: Burns RM, Honkala BH (eds), Silvics of North America vol 1. Conifers. Agricultural Handbook 654. USDA Forest Service, Washington, DC
Montgomery ME, Bentz SE, Olsen RT (2009) Evaluation of hemlock (Tsuga) species and hybrids for resistance to Adelges tsugae (Hemiptera: Adelgidae) using artificial infestation. J Econ Entomol 102:1247–1254
Nelson LA (2012) Geographically distinct Tsuga: Variation in tree physiology, host resistance, and predator response. MS Thesis, Department of Entomology, University of Kentucky, Lexington. 88 p
Nelson LA, Rieske LK (2014) Microclimatic variation within sleeve cages in ecological studies. J Insect Sci (in press)
Nuckolls AE, Wurzburger N, Ford CR, Hendrick RL, Vose JM, Kloeppel BD (2009) Hemlock declines rapidly with hemlock woolly adelgid infestation: impacts on the carbon cycle of southern Appalachian forests. Ecosystems 12:179–190
Orwig DA, Foster DR (1998) Forest response to the introduced hemlock woolly adelgid in southern New England, USA. J Torrey Bot Soc 125:60–73
Packee EC (1990) Tsuga heterophylla. In: Burns RM, Honkala BH (eds), Silvics of North America volume 1. Conifers. Agricultural Handbook 654. USDA Forest Service, Washington, DC
Pontius JA, Hallett RA, Jenkins JC (2006) Foliar chemistry linked to infestation and susceptibility to hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 35:112–120
Radville L, Chaves A, Preisser EL (2011) Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis). J Chem Ecol 37:592–597
Rankin W, Tramer EJ (2002) The gap dynamics of canopy trees of a Tsuga canadensis forest community. Northeast Nat 9:391–406
Ross R, Bennett R, Snyder C, Smith D, Young J, Lemarie D (2003) Influence of eastern hemlock (Tsuga canadensis L.) on fish community structure and function in headwater streams of the Delaware River basin. Ecol Freshw Fish 12:60–65
Snyder CD, Young JA, Lemarie DP, Smith DR (2002) Influence of eastern hemlock (Tsuga canadensis) forests on aquatic invertebrate assemblages in headwater streams. Can J Fish Aquat Sci 59:262–275
Swartley JC (1984) The cultivated hemlocks. Timber Press, Portland, OR
Trotter RT III, Shields KS (2009) Variation in winter survival of the invasive hemlock woolly adelgid (Hemiptera: Adelgidae) across the eastern United States. Environ Entomol 38:577–587
Wang CW (1961) The forests of China with a survey of grassland and desert vegetation. Maria Moors Cabot Foundation Publication 5. Harvard University, Cambridge
Weston PA, Harper RW (2009) Potential of Tsuga spp. from Western North America and Asia as replacements for eastern hemlock (Tsuga canadensis). Arboric Urban Forest 35:5–9
Yorks TE, Jenkins JC, Leopold DJ, Raynal DJ, Orwig DA (2000) Influences of eastern hemlock mortality on nutrient cycling. In: Proceedings: symposium on sustainable management of hemlock ecosystems in eastern North America. Northeastern Research Station, pp 126–133
Yorks TE, Leopold DJ, Raynal DJ (2003) Effects of Tsuga canadensis mortality on soil water chemistry and understory vegetation: possible consequences of an invasive insect herbivore. Can J For Res 33:1525–1537
Young RF, Shields KS, Berlyn GP (1995) Hemlock woolly adelgid (Homoptera, Adelgidae)—stylet bundle insertion and feeding sites. Ann Entomol Soc Am 88:827–835
Zvereva EL, Lanta V, Kozlov MV (2010) Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies. Oecologia 163:949–960
Acknowledgments
The authors thank Joshua Adkins, Luke Dodd, Ignazio Graziosi, Abe Levin-Nielsen and Melanie Sprinkle for assistance in the field, and Millie Hamilton who provided assistance with the LICOR 6400 portable photosynthesis system. Dan Potter and John Obrycki reviewed earlier versions of this manuscript. This work was supported by USDA Forest Service FHP EM and MacIntire Stennis funds from the Kentucky Agricultural Experiment Station and is published as Experiment Station #12-08-114.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Handling Editors: Walter Carson and Heikki Hokkanen.
Rights and permissions
About this article
Cite this article
Nelson, L.A., Dillaway, D.N. & Rieske, L.K. Effect of an exotic herbivore, Adelges tsugae, on photosynthesis of a highly susceptible Tsuga host, with notes on conspecifics. Arthropod-Plant Interactions 8, 9–15 (2014). https://doi.org/10.1007/s11829-013-9285-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-013-9285-9