Abstract
Aside from the larger question of which traits make introduced species invasive, there is the practical concern of understanding the ecology of established invasives. An ecological understanding of invaders allows us to better identify invasible habitats and know the advantages and disadvantages an invader holds in relation to natives. This gives insights on how the invader will interact with natives, and how it might fare over time. Throughout eastern North America Amur honeysuckle (Lonicera maackii (Rupr.) Maxim) is a notorious invader of forests and forest edges. The species inflicts harm on individual species, communities, and ecosystem functions. Lonicera appears in forests across a continuum of light conditions. It possesses considerable shade tolerance, although the extent and nature of this trait has been rarely contrasted with native species. Lonicera appears to be less abundant and slower growing under the closed canopy of the forest interior. Forests on mesic sites, especially those with closed sugar maple (Acer saccharum Marshall.) canopies or dense subcanopies have especially dim understories, perhaps posing a significant limitation on carbon gain in Lonicera. I compared the photosynthetic responses, leaf characteristics, and leaf area ratios (LAR) of Lonicera to two shade tolerant native understory shrubs, Asimina triloba Adans. (pawpaw) and Lindera benzoin Thunb. (spicebush). Lonicera had comparable light responses measured on a leaf area basis, but mass-based measurements show it is less efficient paying back carbon invested in leaf tissue. This arises because Lonicera does not adjust specific leaf mass downward to the level of Asimina and Lindera in deep shade. LAR is distinctly higher in Asimina and Lindera, suggesting higher rates of carbon gain in the native species. Because photosynthesis is only one of many other physiological, demographic, and community-level processes in play, we should not necessarily assume lesser success for Lonicera in deep shade.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data are available from the author.
References
Alexander HD, Siegert C, Brewer JS, Kreye J, Lashley MA, McDaniel JK, Paulson AK, Renninger HJ, Varner JM (2021) Mesophication of oak landscapes: evidence, knowledge gaps, and future research. Bioscience 71:531–542. https://doi.org/10.1093/biosci/biaa169
Allana BF, Dutra HP, Goessling LS, Barnett K, Chasea JM, Marquis RJ, Pang G, Storch GA, Thach RE, Orrock JL (2010) Invasive Lonicera eradication reduces tick-borne disease risk by altering host dynamics. Proc Natl Acad Sci USA 107:18523–18527. https://doi.org/10.1073/pnas.1008362107
Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of an invasive shrub. Biol Invasions 8:1013–1022. https://doi.org/10.1007/s10530-005-3634-2
Bartuszevige AM, Gorchov DL, Raab L (2006) The relative importance of landscape and community features in the invasion of an exotic shrub in a fragmented landscape. Ecography 29:213–222. https://doi.org/10.1111/j.2006.0906-7590.04359.x
Baumer M, Runkle JR (2010) Tree seedling establishment under the native shrub, Asimina triloba. Castanea 75:421–432
Bjorkman O (ed) (1981) Responses to different quantum flux densities. Volume 12A: Responses to the physical environment. Springer, New York
Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355–377. https://doi.org/10.1146/annurev.pp.28.060177.002035
Braun EL (1950) Deciduous forests of eastern North America. Hafner Press, New York
Castellano SM, Gorchov DL (2013) White-tailed deer (Odocoileus virginianus) disperse seeds of the invasive shrub, Amur honeysuckle (Lonicera maackii). Nat Areas J 33:78–80. https://doi.org/10.3375/043.033.0109
Chabot BF, Chabot JF (1977) Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26:363–377
Collier MW, Vankat JL (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71. https://doi.org/10.1674/0003-0031(2002)147[0060:DPRAAB]2.0.CO;2
Curtis JT (1959) The vegetation of Wisconsin. University of Wisconsin Press, Madison
Davidson DW (1966) Response of six shrub species to light regimes in two controlled-environment rooms. Bull Torrey Bot Club 93:432–437
Dornbos DL Jr, Martzke MR, Gries K, Hesselink R (2016) Physiological competitiveness of autumn olive compared with native woody competitors in open field and forest understory. For Ecol Manage 372:101–108. https://doi.org/10.1016/j.foreco.2016.03.051
Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA): Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs. Simon Fraser University, Burnaby
Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362. https://doi.org/10.1038/nature11056
Gates DM (1980) Biophysical ecology. Springer-Verlag, New York
Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92. https://doi.org/10.1071/PP9880063
Gorchov DL (2005) Control of forest invasives and responses of native forest-floor plants: case studies of garlic mustard and Amur honeysuckle. In: Cardina J (ed) Proceedings Ohio Invasive Plant Research Conference: Bridging the Gap Between Land Management and Research. Ohio Agricultural Research and Development Center, Special Circular 196, pp 30–40
Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Midl Nat 144:36–50. https://doi.org/10.1674/0003-0031(2000)144[0036:EOTEIS]2.0.CO;2
Harrington RA, Brown BJ, Reich PB (1989) Ecophysiology of exotic and native shrubs in southern Wisconsin I. Relationship of leaf characteristics, resource availability, and phenology to seasonal patterns of carbon gain. Oecologia 80:356–367. https://doi.org/10.1007/BF00379037
Helsen K, Matsushima H, Somers B, Honnay O (2021) A trait-based approach across the native and invaded range to understand plant invasiveness and community impact. Oikos 130:1001–1013. https://doi.org/10.1111/oik.08034
Henkin MA, Medley KE, Abbitt RJ, Patton JM (2013) Invasion dynamics of nonnative Amur honeysuckle over 18 years in a southwestern Ohio forest. Am Midl Nat 170:335–347. https://doi.org/10.1674/0003-0031-170.2.335
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. https://doi.org/10.1139/b79-163
Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:11117–11124
NIH (National Institutes of Health) (2023) ImageJ: Image processing and analysis in Java. US National Institutes of Health. https://imagej.nih.gov/ij/. Accessed 26 June 2023
Immel DL (2001) Asimina Asimina triloba (L.) Dunal.: USDA, NRCS, National Plant Data Center. https://plants.sc.egov.usda.gov/DocumentLibrary/plantguide/doc/cs_astr.docx. Accessed 20 Dec 2022
Ingold JL, Craycraft M (1983) Avian frugivory on honeysuckle (Lonicera) in southwestern Ohio in fall. Ohio J Sci 83:256–258
Liang SY, Seagle SW (2002) Browsing and microhabitat effects on riparian forest woody seedling demography. Ecology 83:212–227
Larimore RL, Busemeyer DT, Ebinger JE (2003) Asimina, Asimina triloba (L) Dunal (Annonaceae), in the Prairie Peninsula of Illinois, USA. Nat Areas J 23:356–361
Leeper RA. 2004. Soil Survey of Madison County, Illinois. United States Department of Agriculture, Natural Resources Conservation Service and Illinois Agricultural Experiment Station. https://archive.org/details/MadisonIL2004. Accessed 26 June 2023
Lei TT, Lechowicz MJ (1990) Shade adaptation and shade tolerance in saplings of three Acer species from eastern North America. Oecologia 84:224–228. https://doi.org/10.1007/BF00318275
Leopold A (1933) Game management. Charles Scribner’s Sons, New York
Lieurance D, Landsbergen K (2016) The influence of light habitat on the physiology, biomass allocation, and fecundity of the invasive shrub Amur honeysuckle (Lonicera maackii, Caprifoliaceae). J Torrey Bot Soc 143:415–426. https://doi.org/10.3159/torrey-d-15-00056.1
Loomis JD, Matter SF, Cameron GN (2015) Effects of invasive Amur honeysuckle (Lonicera maackii) and white-tailed deer (Odocoileus virginianus) on survival of sugar maple seedlings in a southwestern Ohio forest. Am Midl Nat 174:65–73. https://doi.org/10.1674/0003-0031-167.2.256
Luken JO (1988) Population structure and biomass allocation of the naturalized shrub Lonicera maackii (Rupr.) Maxim. in forest and open habitats. Am Midl Nat 119:258–267. https://doi.org/10.2307/2425809
Luken JO, Goessling N (1995) Seedling distribution and potential persistence of the exotic shrub Lonicera maackii in fragmented forests. Am Midl Nat 133:124–130
Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24. https://doi.org/10.2307/1312651
Luken JO, Kuddes LM, Tholemeier TC, Haller DM (1997) Comparative responses of Lonicera maackii (Amur honeysuckle) and Lindera benzoin (Lindera) to increased light. Am Midl Nat 138:331–343
Mathakutha R, Steyn C, le Roux PC, Blom IJ, Chown SL, Daru BH, Ripley BS, Louw A, Greve M (2019) Invasive species differ in key functional traits from native and non-invasive alien plant species. J Veg Sci 30:994–1006. https://doi.org/10.1111/jvs.12772
Maynard-Bean E, Kaye M, Wagner T, Burkhart EP (2020) Citizen scientists record novel leaf phenology of invasive shrubs in eastern US forests. Biol Invasions 22:3325–3337. https://doi.org/10.1007/s10530-020-02326-1
McEwan RW, Arthur MA, Alverson SE (2012) Throughfall chemistry and soil nutrient effects of the invasive shrub Lonicera maackii in deciduous forests. Am Midl Nat 168:43–55. https://doi.org/10.1674/0003-0031-168.1.43
McNeish RE, McEwan RW (2016) A review on the invasion ecology of Amur honeysuckle (Lonicera maackii, Caprifoliaceae) a case study of ecological impacts at multiple scales. J Torrey Bot Soc 143:367–385. https://doi.org/10.3159/torrey-d-15-00049.1
McNeish RE, Moore EM, Benbow ME, McEwan RW (2015) Removal of the invasive shrub, Lonicera maackii, from riparian forests influences headwater stream biota and ecosystem function. River Res Appl 31:1131–1139. https://doi.org/10.1002/rra.2808
Meiners SJ (2007) Apparent competition: an impact of exotic shrub invasion on tree regeneration. Biol Invasions 9:849–855. https://doi.org/10.1007/s10530-006-9086-5
Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375. https://doi.org/10.1007/s00442-004-1518-2
Mooney EH, Niesenbaum RA (2012) Population-specific responses to light influence herbivory in the understory shrub Lindera benzoin. Ecology 93:2683–2692
Nesom G (2002) LINDERA Lindera benzoin (L.) Blume: USDA, NRCS, National Plant Data Center. https://plants.usda.gov/home/plantProfile?symbol=LIBE3. Access 23 Mar 2023
Niesenbaum RA (1992) The effects of light environment on herbivory and growth in the dioecious shrub Lindera benzoin (Lauraceae). Am Midl Nat 128:270–275
Nowacki GJ, Abrams MD (2008) The demise of fire and “mesophication” of forests in the eastern United States. Bioscience 58:123–138. https://doi.org/10.1641/b580207
O’Connell E, Savage J (2020) Extended leaf phenology has limited benefits for invasive species growing at northern latitudes. Biol Invasions 22:2957–2974. https://doi.org/10.1007/s10530-020-02301-w
Olson MG, Keeley MT (2018) Controlling dense layers of Asimina (Asimina triloba) in mesic upland forest understories. For Sci 64:324–329. https://doi.org/10.1093/forsci/fxx015
Orrock JL, Dutra HP, Marquis RJ, Barber N (2015) Apparent competition and native consumers exacerbate the strong competitive effect of an exotic plant species. Ecology 96:1052–1061. https://doi.org/10.1890/14-0732.1
Pattison RR, Goldstein G, Ares A (1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117:449–459
Rejmanek M (1996) A theory of seed plant invasiveness: the first sketch. Biol Cons 78:171–181. https://doi.org/10.1016/0006-3207(96)00026-2
Rogstad RH, Wolff K, Schaal BA (1991) Geographical variation in Asimina triloba Dunal (Annonaceae) revealed by the M13 “DNA fingerprinting” probe. Am J Bot 78:1391–1396. https://doi.org/10.2307/2445277
Schulz KE, Wright J (2015) Reproduction of invasive Amur honeysuckle (Lonicera maackii) and the arithmetic of an extermination strategy. Restor Ecol 23:900–908. https://doi.org/10.1111/rec.12260
Sena K, Gauger L, Johnson T, Shirkey F, Caldbeck W, Hammock J, Kim A, Mazza B, Pethtel I, Leuenberger W (2021) Honeysuckle (Lonicera maackii) presence is associated with reduced diversity and richness of flowering spring flora in central Kentucky. Nat Areas J 41:249–257. https://doi.org/10.3375/20-41
Slater MA, Anderson RC (2014) Intensive selective deer browsing favors success of Asimina triloba (Asimina) a native tree species. Nat Areas J 34:178–187. https://doi.org/10.3375/043.034.0207
Trammell TLE, Ralston HA, Scroggins SA, Carreiro MM (2012) Foliar production and decomposition rates in urban forests invaded by the exotic invasive shrub, Lonicera maackii. Biol Invasions 14:529–545. https://doi.org/10.1007/s10530-011-0093-9
Tukey JW (1949) Comparing individual means in the analysis of variance. Biometrics 5:99–114
Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Vellend M (2002) A pest and an invader: white-tailed deer (Odocoileus virginianus Zimm.) as a seed dispersal agent for honeysuckle shrubs (Lonicera L.). Nat Areas J 22:230–234
Veres JS, Pickett STA (1982) Branching patterns of Lindera benzoin beneath gaps and closed canopies. New Phytol 91:767–772
Walters MB, Kruger EL, Reich PB (1993) Growth, biomass distribution and CO2 exchange of northern hardwood seedlings in high and low light: relationships with successional status and shade tolerance. Oecologia 94:7–16. https://doi.org/10.1007/BF00317294
Woodward FI (1990) From ecosystems to genes: the importance of shade tolerance. Trends Ecol Evol 5:111–115. https://doi.org/10.1016/0169-5347(90)90164-9
Xu C-Y, Griffin KL, Schuster WSF (2007) Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154:11–21
Funding
Gas analyzer calibration and maintenance were supported by a Seed Grant for Transitional and Exploratory Projects awarded to Kurt Schulz by the Graduate School of Southern Illinois University Edwardsville.
Author information
Authors and Affiliations
Contributions
Kurt Schulz wrote the main manuscript and prepared all figures and tables. KS conceived the project, collected, and analyzed the data, and wrote the manuscript. Special thanks to Anh Nguyen (Southern Illinois University Edwardsville) for considerable assistance with field data collection.
Corresponding author
Ethics declarations
Conflict of interest
The author has no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Norris Muth.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Schulz, K.E. Photosynthesis and shoot allocation of amur honeysuckle and two native shrubs in deep shade. Plant Ecol 224, 921–930 (2023). https://doi.org/10.1007/s11258-023-01347-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-023-01347-9