The influence of riparian invasion by the terrestrial shrub Lonicera maackii on aquatic macroinvertebrates in temperate forest headwater streams

Abstract

The ecology of headwater streams is tightly linked to the riparian zone through organic matter subsidies which are highly susceptible to alteration due to biological invasion. Lonicera maackii is a non-native shrub that is a highly successful invader of headwater stream riparian zones in the American Midwest. We assessed effects on benthic macroinvertebrates across a gradient of invasion intensity from references sites with minimal invasion to a site that had a very heavy invasion. Benthic macroinvertebrates were sampled throughout the year and compositional differences were assessed using Non-metric Multidimensional Scaling ordination, and by comparing the prevalence of sensitive (Ephemeroptera, Plectoptera, and Trichoptera: EPT) and tolerant (Chironomidae) macroinvertebrate taxa. We found strong evidence of variation among macroinvertebrate communities across the invasion gradient (ANOSIM R = 0.215, P = 0.004) and particularly strong separation between one of our reference sites with minimal invasion and the site with the heaviest invasion. Analysis of EPT taxa indicated a significant overall effect and pairwise comparisons indicated that the site with the heaviest invasion had the lowest percentage of sensitive taxa (P < 0.05). Our analysis of chironomids did not yield a statistically discernable effect, although the pattern of the data suggest higher dominance in the site with the heaviest invasion. These stream-scale results bolster prior laboratory and field experiments and provide evidence that terrestrial invasion of L. maackii impacts the benthic community present in headwater streams. These results provide impetus to re-focus stream management recommendations to include practices that control invasive plants in riparian forests.

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References

  1. Arthur MA, Bray SR, Kuchle CR, McEwan RW (2012) The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecol 213:1571–1582

    Article  Google Scholar 

  2. Bailey JK, Schweitzer JA, Whitham TG (2001) Salt cedar negatively affects biodiversity of aquatic macroinvertebrates. Wetlands 21:442–447

    Article  Google Scholar 

  3. Barbour MT, Gerritsen J, Snyder BD, Stribling JB (1999) Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish. US Environmental Protection Agency, Office of Water, Washington, vol 339

    Google Scholar 

  4. 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

    Article  Google Scholar 

  5. Baxter CV, Fausch KD, Saunders CW (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220

    Article  Google Scholar 

  6. Borth EB, Custer KW, McEwan RW (2018) Lethal effects of leaf leachate from the non-native invasive shrub Amur honeysuckle (Lonicera maackii) on a model aquatic organism (Hyalella azteca). Ecoscience 2:189–197

    Article  Google Scholar 

  7. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  8. Clinton BD (2011) Stream water responses to timber harvest: riparian buffer width effectiveness. For Ecol Manag 261:979–988

    Article  Google Scholar 

  9. Collier MH, Vankat JL, Hughes MR (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71

    Article  Google Scholar 

  10. Custer KW, Borth EB, Mahoney SD, McEwan RW (2017) Lethal and sublethal effects of novel terrestrial subsidies from an invasive shrub (Lonicera maackii) on stream macroinvertebrates. Freshw Sci 36:750–759

    Article  Google Scholar 

  11. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296

    Article  Google Scholar 

  12. Fei S, Phillips J, Shouse M (2014) Biogeomorphic impacts of invasive species. Annu Rev Ecol Evol Syst 45:69–87

    Article  Google Scholar 

  13. Ferreira WR, Ligeiro R, Macedo DR, Hughes RM, Kaufmann PR, Oliveira LG, Callisto M (2014) Importance of environmental factors for the richness and distribution of benthic macroinvertebrates in tropical headwater streams. Freshw Sci 33:860–871

    Article  Google Scholar 

  14. Gorchov DL, Trisel DE (2003) Competitive effects of the invasive shrub, Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings. Plant Ecol 166:13–24

    Article  Google Scholar 

  15. Gould AM, 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

    Article  Google Scholar 

  16. Gregory SV, Swanson FJ, Mckee WA, Kenneth W, Swanson J, Cummins KW (1991) An Ecosystem Perspective of Riparian Zones Focus on links between land and water. Bioscience 41:540–551

    Article  Google Scholar 

  17. Harner MJ, Crenshaw CL, Abelho M, Stursova M, Shah JJF, Sinsabaugh RL (2009) Decomposition of leaf litter from a native tree and an actinorhizal invasive across riparian habitats. Ecol Appl 19:1135–1146

    PubMed  Article  Google Scholar 

  18. Hartman KM, McCarthy BC (2004) Restoration of a forest understory after the removal of an invasive shrub, Amur honeysuckle (Lonicera maackii). Restor Ecol 12:154–165

    Article  Google Scholar 

  19. Hilsenhoff WL (1988) Rapid field assessment of organic pollution with a family-level biotic index. J N Am Benthol Soc 7:65–68

    Article  Google Scholar 

  20. Hultine KR, Belnap J, van Riper III, Ehleringer C, Dennison JR, Lee PE, Nagler ME, Snyder PL, Uselman KA, West SM, J.B (2010) Tamarisk biocontrol in the western United States: ecological and societal implications. Front Ecol Environ 8:467–474

    Article  Google Scholar 

  21. Janssens De Bisthoven, L, Gerhardt A, Soares AMVM (2005) Chironomidae larvae as bioindicators of an acid mine drainage in Portugal. Hydrobiologia 532:181–191

    Article  Google Scholar 

  22. Lenat DR (1983) Chironomid taxa richness: natural variation and use in pollution assessment. Freshw Invertebr Biol 2:192–198

    Article  Google Scholar 

  23. Lenth R, Singmann H, Love J (2018) Emmeans: Estimated marginal means, aka least-squares means. R package version, 1(1)

  24. Lieurance D, Cipollini D (2012) Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range. Biol Invasions 14:863–873

    Article  Google Scholar 

  25. Lieurance D, Chakraborty S, Whitehead SR, Powell JR, Bonello P, Bowers MD, Cipollini D (2015) Comparative herbivory rates and secondary metabolite profiles in the leaves of native and non-native Lonicera species. J Chem Ecol 41:1069–1079

    CAS  PubMed  Article  Google Scholar 

  26. Likens GE, Bormann FH, Pierce RS, Reiners WA (1978) Recovery of a deforested ecosystem. Science 199:492–496

    CAS  PubMed  Article  Google Scholar 

  27. Luken JO, Mattimiro DT (1991) Habitat-specific resilience of the invasive shrub Amur honeysuckle (Lonicera maackii) during repeated clipping. Ecol Appl 1:104–109

    PubMed  Article  Google Scholar 

  28. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24

    Article  Google Scholar 

  29. McEwan RW, Birchfield MK, Schoergendorfer A, Arthur MA (2009) Leaf phenology and freeze tolerance of the invasive shrub Amur honeysuckle and potential native competitors. J Torrey Bot Soc 136:212–220

    Article  Google Scholar 

  30. McEwan RW, Arthur-Paratley LG, Rieske LK, Arthur MA (2010) A multi-assay comparison of seed germination inhibition by Lonicera maackii and co-occurring native shrubs. Flora 205: 475–483

    Article  Google Scholar 

  31. McEwan RW, Rieske LK, Arthur MA (2009b) Potential interactions between invasive woody shrubs and the gypsy moth (Lymantria dispar), an invasive insect herbivore. Biol Invasions 11:1053–1058

    Article  Google Scholar 

  32. McNeish RE, Benbow ME, McEwan RW (2012) Riparian forest invasion by a terrestrial shrub (Lonicera maackii) impacts aquatic biota and organic matter processing in headwater streams. Biol Invasions 14:1881–1893

    Article  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. McNeish RE, Benbow ME, McEwan RW (2017) Removal of the invasive shrub, Lonicera maackii (Amur Honeysuckle), from a headwater stream riparian zone shifts taxonomic and functional composition of the aquatic biota. Invasive Plant Sci Manag 10:232–246

    Article  Google Scholar 

  35. Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375

    PubMed  Article  PubMed Central  Google Scholar 

  36. Mineau MM, Baxter CV, Marcarelli AM, Minshall GW (2012) An invasive riparian tree reduces stream ecosystem efficiency via a recalcitrant organic matter subsidy. Ecology 93:1501–1508

    PubMed  Article  PubMed Central  Google Scholar 

  37. Moore A, Palmer MA (2005) Invertebrate biodiversity in agricultural and urban headwater streams: implications for conservation and management. Ecol Appl 15:1169–1177

    Article  Google Scholar 

  38. Ohio EPA (2018) Field methods for evaluating primary headwater streams in Ohio. Version 4.0. Division of Surface Water. Environmental Protection Agency. State of Ohio. Available from: https://www.epa.state.oh.us/Portals/35/rules/PHWHManual_2018_Ver_4%200_10-22-18.pdf

  39. Oksanen JF, Blanchet G, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17-4. http://cran.r-project.org

  40. Pinheiro J, Bates D, DebRoy S, Sarkar D (2019) R Core Team. 2019. nlme: linear and nonlinear mixed effects models. R package version 3.1–141. Available at https://svn.r-project.org/R-packages/trunk/nlme/

  41. Peck DV, Herlihy AT, Hill BH, Hughes RM, Kaufmann PR, Klemm DJ, Lazorchak JM, McCormick FH, Peterson SA, Ringold PL, Magee T, Cappaert MR (2006) Environmental Monitoring and Assessment Program-Surface waters western pilot study: field operations manual for wadable streams. Environmental Monitoring Assessment Program: EPA/620/R, 275

  42. Phillips MJ, Swift LW Jr, Blinn CR (2000) Best management practices for riparian areas. In: Verry ES, Hornbeck JW, Dolloff CA (eds) Riparian management of forests of Continental Eastern United States. Lewis Publishers, Boca Raton, pp 272–285

    Google Scholar 

  43. Polis GA, Strong DR (1996) Food web complexity and community dynamics. Am Nat 147: 813–846

    Article  Google Scholar 

  44. Pond GJ, Passmore ME, Borsuk FA, Reynolds L, Rose CJ (2008) Downstream effects of mountaintop coal mining: comparing biological conditions using family- and genus-level macroinvertebrate bioassessment tools. J N Am Benthol Soc 27:717–737

    Article  Google Scholar 

  45. Poulette MM, Arthur MA (2012) The impact of the invasive shrub Lonicera maackii on the decomposition dynamics of a native plant community. Ecol Appl 22:412–424

    PubMed  Article  PubMed Central  Google Scholar 

  46. Rae JG (1989) Chironomid midges as indicators of organic pollution in the Scioto River Basin, Ohio. Ohio J Sci 89:5–9

    CAS  Google Scholar 

  47. Reinhart KO, VandeVoort R (2006) Effect of native and exotic leaf litter on macroinvertebrate communities and decomposition in a western Montana stream. Divers Distrib 12:776–781

    Article  Google Scholar 

  48. Ricciardi A, Atkinson SK (2004) Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecol Lett 7:781–784

    Article  Google Scholar 

  49. Richardson DM, Holmes PM, Esler KJ, Galatowitsch SM, Stromberg JC, Kirkman SP, Pyšek P, Hobbs RJ (2007) Riparian vegetation: degradation, alien plant invasions, and restoration prospects. Divers Distrib 13:126–139

    Article  Google Scholar 

  50. Roth TR, Westhoff MC, Huwald H, Huff JA, Rubin JF, Barrenetxea G, Vetterli M, Parriaux A, Selker JS, Parlange MB (2010) Stream temperature response to three riparian vegetation scenarios by use of a distributed temperature validated model. Environ Sci Technol 44:2072–2078

    CAS  PubMed  Article  Google Scholar 

  51. Rowekamp EC, Chapman JI, McEwan RW (2020) Assessing the influence of riparian invasion by the shrub Lonicera maackii on terrestrial subsidies to headwater streams. Acta Oecologica. https://doi.org/10.1016/j.actao.2020.103580

    Article  Google Scholar 

  52. Silva DRO, Ligeiro R, Hughes RM, Callisto M (2014) Visually determined stream mesohabitats influence benthic macroinvertebrate assessments in headwater streams. Environ Monit Assess 186:5479–5488

    CAS  PubMed  Article  Google Scholar 

  53. Smith EP, Voshell JR Jr (1997) Studies of benthic macroinvertebrates and fish in streams within EPA Region 3 for development of biological indicators of ecological condition. Part 1, benthic macroinvertebrates. Report to U.S. Environmental Protection Agency Cooperative Agreement CF821462010. EPA, Washington, DC. Available from: http://www.epa.state.oh.us/portals/35/volunteermonitoring/references/SmithandVoshell1997.pdf

  54. Strauss SY, Webb CO, Salamin N (2006) Exotic taxa less related to native species are more invasive. Proc Natl Acad Sci USA 103:5841–5845

    CAS  PubMed  Article  Google Scholar 

  55. Swan CM, Healey B, Richardson DC (2008) The role of native riparian tree species in decomposition of invasive tree of heaven (Ailanthus altissima) leaf litter in an urban stream. Ecoscience 15:27–35

    Article  Google Scholar 

  56. Swank WT, Vose J, Elliott KJ (2001) Long-term hydrologic and water quality responses following commercial clearcutting of mixed hardwoods on a southern Appalachian catchment. For Ecol Manag 143:163–178

    Article  Google Scholar 

  57. Tabacchi E, Planty-Tabacchi AM (2003) Recent changes in riparian vegetation: possible consequences on dead wood processing along rivers. River Res Appl 19:251–263

    Article  Google Scholar 

  58. Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML (2010) A review of allochthonous organic matter dynamics and metabolism in streams. J N Am Benthol Soc 29:118–146

    Article  Google Scholar 

  59. USEPA (2006) Wadeable streams assessment. USEPA-841‐B‐06-002. USEPA, Washington, DC

    Google Scholar 

  60. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137

    Article  Google Scholar 

  61. Voshell JR Jr (2002) A guide to common freshwater invertebrates of North America. McDonald & Woodward, Blacksburg

    Google Scholar 

  62. Wallace JB (1996) The role of macroinvertebrates in stream ecosystem function. Annu Rev Entomol 41:115–139

    CAS  PubMed  Article  Google Scholar 

  63. Wallace JB, Eggert SL, Meyer JL, Webster JR (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–105

    CAS  Article  Google Scholar 

  64. Wallace JB, Eggert SL, Meyer JL, Webster JR, Sobczak WV (2015) Stream invertebrate productivity linked to forest subsidies: 37 stream-years of reference and experimental data. Ecology 96:1213–1228

    PubMed  Article  Google Scholar 

  65. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  66. Woods MJ, Roberson E, Cipollini D, Rúa MA (2019) White-tailed deer and an invasive shrub facilitate faster carbon cycling in a forest ecosystem. For Ecol Manag 448:104–111

    Article  Google Scholar 

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Acknowledgements

We thank Aullwood Audubon Center, Miami County Park District, and the Five Rivers MetroParks for providing site access and logistical support. We would like to thank Jenea Adams, Chelsie Baylor, Taylor Buskey, Marcella Domka, Shante Eisele, Elise Erhart, Sarah Frankenberg, Abby Hay, Sean Mahoney Celia Montemurri, Joe Murphy, Kyle Murphy, Erin Rowekamp, Katie Schrader and Charlotte Shade for assistance in the field and lab. Funding for this project was provided by the University of Dayton Honors Program and an award from the National Science Foundation (DEB 1352995).

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Correspondence to Ryan W. McEwan.

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Little, M.N., Custer, K.W., Borth, E.B. et al. The influence of riparian invasion by the terrestrial shrub Lonicera maackii on aquatic macroinvertebrates in temperate forest headwater streams. Biol Invasions 23, 25–35 (2021). https://doi.org/10.1007/s10530-020-02349-8

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Keywords

  • Amur honeysuckle
  • River continuum concept
  • Organic matter subsidies
  • Terrestrial-aquatic linkages
  • Exotic species
  • EPT taxa