Advertisement

Aquatic Sciences

, 81:11 | Cite as

Changes in benthic invertebrate communities of central Appalachian streams attributed to hemlock woody adelgid invasion

  • Kristen M. DiesburgEmail author
  • S. Mažeika P. Sullivan
  • David W. P. Manning
Research Article

Abstract

Eastern hemlock trees (Tsuga canadensis [L.] Carr.) often dominate riparian vegetation of central Appalachian headwater streams, and the invasive hemlock woolly adelgid (Adelges tsugae Annand; HWA) has decimated hemlock stands in this region. Although research concerning HWA impacts on soil, hydrology, and forest structure is emerging, associated changes in stream structure and function are not as well documented. We quantified HWA-invasion effects on benthic macroinvertebrate communities in 21 headwater streams across Ohio, West Virginia, and Virginia (USA) representing unimpacted, moderate invasion, and severe invasion, respectively. We observed differences in benthic macroinvertebrate community composition; severely invaded sites exhibited the highest diversity, whereas moderate sites had the lowest diversity. The composition of macroinvertebrate functional feeding groups exhibited shifts as well. For example, the relative abundance of herbivorous invertebrates increased from 4% (± 3%) at unimpacted sites to 23% (± 14%) at severely impacted sites. Changes in macroinvertebrate density, diversity, and functional-group composition were associated with sediment grainsize distribution (proportion bedrock and D84), large-wood characteristics (volume and density), and nutrient concentrations (PO4 and NH4). Our results suggest that in-stream physical and chemical alterations associated with HWA-invasion and subsequent hemlock decline are associated with changes in stream invertebrate diversity and trophic relationships. We demonstrate how a pervasive terrestrial invader can influence in-stream biotic communities.

Keywords

Aquatic insects Aquatic-terrestrial linkages Invasive species Stream ecosystems Water chemistry 

Notes

Acknowledgements

Research support was provided by state and federal funds appropriated to The Ohio State University, Ohio Agricultural Research and Development Center (OARDC) through the OARDC Research Enhancement Competitive Grants Program (SMPS). We also wish to thank members of the Stream and River Ecology (STRIVE) Lab for their assistance in the lab and the field, as well as additional support from P. Soltesz, Dr. P.C. Goebel, and Dr. K. Jaeger.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

27_2018_607_MOESM1_ESM.xlsx (84 kb)
Online Resource 1 Raw data including macroinvertebrate taxa, sampling dates, microhabitat, and functional feeding group designation (XLSX 84 KB)

References

  1. Adkins JK, Rieske LK (2015a) A terrestrial invader threatens a benthic community: potential effects of hemlock woolly adelgid-induced loss of eastern hemlock on invertebrate shredders in headwater streams. Biol Invasions 17(4):1163–1179.  https://doi.org/10.1007/s10530-014-0786-y CrossRefGoogle Scholar
  2. Adkins JK, Rieske LK (2015b) Benthic collector and grazer communities are threatened by hemlock woolly adelgid-induced eastern hemlock loss. Forests 6(8):2719–2738.  https://doi.org/10.3390/f6082719 CrossRefGoogle Scholar
  3. Angermeier PL, Wheeler AP, Rosenberger AE (2004) A conceptual framework for assessing impacts of roads on aquatic biota. Fisheries 29(12):19–29CrossRefGoogle Scholar
  4. Benke A, Wallace JB (2003) Influence of wood on invertebrate communities in streams and rivers. In: Gregory SV, Boyer KL, Gurnell AM (eds) The ecology and management of wood in world rivers. American Fisheries Society 37, Symposium. Bethesda, Maryland, pp 149–177Google Scholar
  5. Brantley S, Ford CR, Vose JM (2013) Future species composition will affect forest water use after loss of eastern hemlock from southern Appalachian forests. Ecol Appl 23(4):777–790.  https://doi.org/10.1890/12-0616.1 CrossRefPubMedGoogle Scholar
  6. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Method Res 33(2):261–304.  https://doi.org/10.1177/0049124104268644 CrossRefGoogle Scholar
  7. Case BS, Buckley HL, Barker-Plotkin AA, Orwig DA, Ellison AM (2017) When a foundation crumbles: forecasting forest dynamics following the decline of the foundation species Tsuga canadensis. Ecosphere 8(7):e01893.  https://doi.org/10.1002/ecs2.1893 CrossRefGoogle Scholar
  8. Cessna JF, Nielsen C (2012) Influences of hemlock woolly adelgid–induced stand-level mortality on nitrogen cycling and stream water nitrogen concentrations in southern Pennsylvania. Castanea 77(2):127–135.  https://doi.org/10.2179/11-025 CrossRefGoogle Scholar
  9. Costigan KH, Soltesz PJ, Jaeger KL (2015) Large wood in central Appalachian headwater streams: controls on and potential changes to wood loads from infestation of hemlock woolly adelgid. Earth Surf Proc Land 40(13):1746–1763.  https://doi.org/10.1002/esp.3751 CrossRefGoogle Scholar
  10. Cross WF, Wallace JB, Rosemond AD, Eggert SL (2006) Whole-system nutrient enrichment increases secondary production in a detritus-based ecosystem. Ecology 87(6):1556–1565.  https://doi.org/10.1890/0012-9658(2006)87[1556:WNEISP]2.0.CO;2 CrossRefPubMedGoogle Scholar
  11. Daley MJ, Phillips NG, Pettijohn C, Hadley JL (2007) Water use by eastern hemlock (Tsuga canadensis) and black birch (Betula lenta): implications of effects of the hemlock woolly adelgid. Can J For Res 37(10):2031–2040.  https://doi.org/10.1139/X07-045 CrossRefGoogle Scholar
  12. Davies KF, Chesson P, Harrison S, Inouye BD, Melbourne BA, Rice KJ (2005) Spatial heterogeneity explains the scale dependence of the native-exotic diversity relationship. Ecology 86(6):1602–1610.  https://doi.org/10.1890/04-1196 CrossRefGoogle Scholar
  13. DeFerrari CM, Naiman RJ (1994) A multi-scale assessment of the occurrence of exotic plants on the Olympic Peninsula, Washington. J Veg Sci 5(2):247–258.  https://doi.org/10.2307/3236157 CrossRefGoogle Scholar
  14. Dextrase AJ, Mandrak NE (2006) Impacts of alien invasive species on freshwater fauna at risk in Canada. Biol Invasions 8:13–24.  https://doi.org/10.1007/s10530-006-1833-0 CrossRefGoogle Scholar
  15. Ellison AM, Banks MS, Clinton BD, Colburn EA, Elliott K, Ford CR et al (2005) Loss of foundation species consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486.  https://doi.org/10.2307/3868635 CrossRefGoogle Scholar
  16. Evans AM, Gregoire TG (2007) A geographically variable model of hemlock woolly adelgid spread. Biol Invasions 9:369–382.  https://doi.org/10.1007/s10530-006-9039-z CrossRefGoogle Scholar
  17. Evans DM, Dolloff CA, Aust WM, Villamagna AM (2012) Effects of eastern hemlock decline on large wood loads in streams of the Appalachian mountains. J Am Water Resour Assoc 48(2):266–276.  https://doi.org/10.1111/j.1752-1688.2011.00610.x CrossRefGoogle Scholar
  18. Feld CK, Segurado P, Gutiérrez-Cánovas C (2016) Analysing the impact of multiple stressors in aquatic biomonitoring data: a ‘cookbook’ with applications in R. Sci Total Environ 573:1320–1339.  https://doi.org/10.1016/j.scitotenv.2016.06.243 CrossRefPubMedGoogle Scholar
  19. Ford CR, Vose JM (2007) Tsuga canadensis (L.) Carr. mortality will impact hydrologic processes in southern Appalachian forest ecosystems. Ecol Appl 17(4):1156–1167.  https://doi.org/10.1890/06-0027 CrossRefPubMedGoogle Scholar
  20. Ford CR, Elliott KJ, Clinton BD, Kloeppel BD, Vose JM (2012) Forest dynamics following eastern hemlock mortality in the southern Appalachians. Oikos 121(4):523–536.  https://doi.org/10.1111/j.1600-0706.2011.19622.x CrossRefGoogle Scholar
  21. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10.  https://doi.org/10.1023/A:1009895103017 CrossRefGoogle Scholar
  22. Glime JM (1968) Ecological observations on some bryophytes in Appalachian Mountain streams. Castanea 33(4):300–325Google Scholar
  23. Gurtz ME, Wallace JB (1984) Substrate-mediated response of stream invertebrates to disturbance. Ecology 65(5):1556–1569.  https://doi.org/10.2307/1939135 CrossRefGoogle Scholar
  24. Hadley JL (2000) Understory microclimate and photosynthetic response of saplings in an old-growth eastern hemlock (Tsuga canadensis L.) forest. Ecoscience 7:66–72.  https://doi.org/10.1080/11956860.2000.11682573 CrossRefGoogle Scholar
  25. Harrelson CC, Rawlins CL, Potyondy JP (1994) Stream channel reference sites: an illustrated guide to field 408 technique. Gen. Tech. Rep. RM-245. Fort Collins, CO: US Department of Agriculture, Forest Service, 409 Rocky Mountain Forest and Range Experiment Station 245, p 61Google Scholar
  26. Hartman KM, McCarthy BC (2008) Changes in forest structure and species composition following invasion by a non-indigenous shrub, Amur honeysuckle (Lonicera maackii). J Torrey Bot Soc 135(2):245–259CrossRefGoogle Scholar
  27. Hynes HBN (1975) The stream and its valley. Verh Int Ver 19:1–15.  https://doi.org/10.1080/03680770.1974.11896033 CrossRefGoogle Scholar
  28. 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(5):630–645.  https://doi.org/10.1139/x99-034 CrossRefGoogle Scholar
  29. Kennedy TA, Hobbie SE (2004) Saltcedar (Tamarix ramosissima) invasion alters organic matter dynamics in a desert stream. Freshw Biol 49:65–76.  https://doi.org/10.1046/j.1365-2426.2003.01166.x CrossRefGoogle Scholar
  30. Kim J, Hwang T, Schaaf CL, Orwig DA, Boose E, Munger JW (2017) Increased water yield due to the hemlock woolly adelgid infestation in New England. Geophys Res Lett 44(5):2327–2335.  https://doi.org/10.1002/2016GL072327 CrossRefGoogle Scholar
  31. Kondolf GM, Micheli ER (1995) Evaluating stream restoration projects. Environ Manage 19(1):1–15CrossRefGoogle Scholar
  32. Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87(2):419–432.  https://doi.org/10.1890/04-1752 CrossRefPubMedGoogle Scholar
  33. Malanson GP (1993) Riparian landscapes. Cambridge University Press, New YorkCrossRefGoogle Scholar
  34. Martin KL, Goebel PC (2012) Decline in riparian Tsuga canadensis forests of the central Appalachians across an Adelges tsugae invasion chronosequence. J Torrey Bot Soc 139(4):367–378.  https://doi.org/10.3159/TORREY-D-12-00012.1 CrossRefGoogle Scholar
  35. Martin KL, Goebel PC (2013) The foundation species influence of eastern hemlock (Tsuga canadensis) on biodiversity and ecosystem function on the Unglaciated Allegheny Plateau. For Ecol Manag 289:143–152.  https://doi.org/10.1016/j.foreco.2012.10.040 CrossRefGoogle Scholar
  36. McDowell WG, McDowell WH, Byers J (2017) Mass mortality of a dominant invasive species in response to an extreme climate event: implications for ecosystem function. Limnol Oceanogr 62:177–188.  https://doi.org/10.1002/lno.10384 CrossRefGoogle Scholar
  37. Merritt R, Cummins K, Berg M (2008) An introduction to the aquatic insects of North America, 4th edn. Kendall Hunt, DubuqueGoogle Scholar
  38. 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(7):1501–1508.  https://doi.org/10.1890/11-1700.1 CrossRefPubMedGoogle Scholar
  39. Morkeski K (2007) In-stream hemlock twig breakdown and effects of reach-scale twig additions on Appalachian headwater streams. Thesis, Virginia TechGoogle Scholar
  40. Naiman RJ, Decamps H (1997) The ecology of interfaces: riparian zones. Annu Rev Ecol Syst 28:621–658.  https://doi.org/10.1146/annurev.ecolsys.28.1.621 CrossRefGoogle Scholar
  41. Naiman RJ, Decamps H, McClain ME (2010) Riparia: ecology, conservation, and management of streamside communities. Academic Press, BeijingGoogle Scholar
  42. Naimi B, Hamm NA, Groen TA, Skidmore AK, Toxopeus AG (2014) Where is positional uncertainty a problem for species distribution modelling? Ecography 37(2):191–203.  https://doi.org/10.1111/j.1600-0587.2013.00205.x CrossRefGoogle Scholar
  43. Nakamura F, Frederick JS, Wondzell SM (2000) Disturbance regimes of stream and riparian systems-disturbance cascade perspective. Hydrol Process 14:2849–2860CrossRefGoogle Scholar
  44. Northington RM, Webster JR, Benfield EF, Cheever BM, Niederlehner BR (2013) Ecosystem function in Appalachian headwater streams during an active invasion by the hemlock woolly adelgid. PloS One 8:4 e61171.  https://doi.org/10.1371/journal.pone.0061171 CrossRefPubMedGoogle Scholar
  45. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4-2. https://CRAN.R-project.org/package=vegan
  46. 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.  https://doi.org/10.2307/2997232 CrossRefGoogle Scholar
  47. Orwig DA, Foster DR, Mausel DL (2002) Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J Biogeogr 29(10–11):1475–1487.  https://doi.org/10.1046/j.1365-2699.2002.00765.x CrossRefGoogle Scholar
  48. Paradis A, Elkinton J, Hayhoe K, Buonaccorsi J (2008) Role of winter temperature and climate change on the survival and future range expansion of the hemlock woolly adelgid (Adelges tsugae) in eastern North America. Mitig Adapt Strat Glob 13(5–6):541–554.  https://doi.org/10.1007/s11027-007-9127-0 CrossRefGoogle Scholar
  49. Pickett ST (1989) Space-for-time substitution as an alternative to long-term studies. In: Likens GE (ed) Long-term studies in ecology. Springer-Verlag, New York, pp 110–135CrossRefGoogle Scholar
  50. Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144CrossRefGoogle Scholar
  51. Poff NL, Olden JD, Vieira NK, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25(4):730–755.  https://doi.org/10.1899/0887-3593(2006)025%5B0730:FTNONA%5D2.0.CO;2 CrossRefGoogle Scholar
  52. Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316.  https://doi.org/10.1146/annurev.ecolsys.28.1.289 CrossRefGoogle Scholar
  53. Quinn JM, Hickey CW (1990) Magnitude of effects of substrate particle size, recent flooding, and catchment development on benthic invertebrates in 88 New Zealand rivers. NZ J Mar Freshwat Res 24(3):411–427.  https://doi.org/10.1080/00288330.1990.9516433 CrossRefGoogle Scholar
  54. Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291–315.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150429 CrossRefGoogle Scholar
  55. Roberts SW, Tankersley R, Orvis KH (2009) Assessing the potential impacts to riparian ecosystems resulting from hemlock mortality in Great Smoky Mountains National Park. Environ Manage 44(2):335–345.  https://doi.org/10.1007/s00267-009-9317-5 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rogers RS (1978) Forests dominated by hemlock (Tsuga canadensis): distribution as related to site and postsettlement history. Can J Bot 56(7):843–854.  https://doi.org/10.1139/b78-096 CrossRefGoogle Scholar
  57. Rowell TJ, Sobczak WV (2008) Will stream periphyton respond to increases in light following forecasted regional hemlock mortality? J Freshw Ecol 23:33–40.  https://doi.org/10.1080/02705060.2008.9664555 CrossRefGoogle Scholar
  58. Sabo JL, Sponseller R, Dixon M, Grade K, Harms T, Heffernan J et al (2005) Riparian zones increase regional species richness by harboring different not more species. Ecology 86:56–62.  https://doi.org/10.1890/04-0668 CrossRefGoogle Scholar
  59. Schindler DE, Knapp RA, Leavitt PR (2001) Alteration of nutrient cycles and algal production resulting from fish introductions into mountain lakes. Ecosystems 4(4):308–321.  https://doi.org/10.1007/s10021-001-0013-4 CrossRefGoogle Scholar
  60. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  61. Siderhurst LA, Griscom HP, Hudy M, Bortolot ZJ (2010) Changes in light levels and stream temperatures with loss of eastern hemlock (Tsuga canadensis) at a southern Appalachian stream: implications for brook trout. For Ecol Manag 260(10):1677–1688.  https://doi.org/10.1016/j.foreco.2010.08.007 CrossRefGoogle Scholar
  62. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66.  https://doi.org/10.1016/j.tree.2012.07.013 CrossRefPubMedGoogle Scholar
  63. Simpson EH (1949) Measurement of diversity. Nature 163(4148):688.  https://doi.org/10.1038/163688a0 CrossRefGoogle Scholar
  64. Smith B, Wilson JB (1996) A consumer’s guide to evenness indices. Oikos 76:70–82.  https://doi.org/10.2307/3545749 CrossRefGoogle Scholar
  65. Snyder CD, Young J, Smith D, Lemarie D, Ross R, Bennett R (1999) Influence of eastern hemlock on aquatic biodiversity in Delaware Water Gap National Recreation Area. Kearneysville, West VirginiaGoogle Scholar
  66. Snyder CD, Young JA, Lemarié DP, Smith DR (2002) Influence of eastern hemlock (Tsuga canadensis) forests on aquatic invertebrate assemblages in headwater streams. Can J Fish Aquat Sci 59(2):262–275.  https://doi.org/10.1139/F02-003 CrossRefGoogle Scholar
  67. Suberkropp K, Gulis V, Rosemond AD, Benstead JP (2010) Ecosystem and physiological scales of microbial responses to nutrients in a detritus-based stream: results of a 5-year continuous enrichment. Limno Oceanogr 55:149–160.  https://doi.org/10.4319/lo.2010.55.1.0149 CrossRefGoogle Scholar
  68. Sullivan SMP, Watzin MC, Hession WC (2004) Understanding stream geomorphic state in relation to ecological integrity: evidence using habitat assessments and macroinvertebrates. Environ Manage 34(5):669–683.  https://doi.org/10.1007/s00267-004-4032-8 CrossRefPubMedGoogle Scholar
  69. Suren AM (1992) Enhancement of invertebrate food resources by bryophytes in New Zealand alpine headwater streams. New Zeal J Mar Freshw 26(2):229–239.  https://doi.org/10.1080/00288330.1992.9516518 CrossRefGoogle Scholar
  70. Thompson R, Townsend C (2003) Impacts on stream food webs of native and exotic forest: an intercontinental comparison. Ecology 84:145–161.  https://doi.org/10.1890/0012-9658(2003)084%5B0145:IOSFWO%5D2.0.CO;2 CrossRefGoogle Scholar
  71. Vieira NKM, Poff NL, Carlisle DM, Moulton IISR, Koski ML, Kondratieff BC (2006) A database of lotic invertebrate traits for North America, Data Series 187. US Geological Survey, RestonGoogle Scholar
  72. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14(7):702–708.  https://doi.org/10.1111/j.1461-0248.2011.01628.x CrossRefPubMedGoogle Scholar
  73. Walker LR, Wardle DA, Bardgett RD, Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98(4):725–736.  https://doi.org/10.1111/j.1365-2745.2010.01664.x CrossRefGoogle Scholar
  74. Wallace JB, Eggert SL (2009) Benthic invertebrate fauna, small streams. Encycl Inland Waters 2:173–190CrossRefGoogle Scholar
  75. Wallace JB, Webster JR (1996) The role of macroinvertebrates in stream ecosystem function. Annu Rev Entomol 41:115–139.  https://doi.org/10.1146/annurev.en.41.010196.000555 CrossRefPubMedGoogle Scholar
  76. Ward JS, Montgomery ME, Cheah CAS, Onken BP, Cowles RS (2004) Eastern hemlock forests: Guidelines to minimize the impacts of hemlock woolly adelgid (NA-TP-03-04) Morgantown, WVGoogle Scholar
  77. Webster J, Morkeski K, Wojculewski C, Niederlehner B, Benfield E, Elliott K (2012) Effects of hemlock mortality on streams in the southern Appalachian Mountains. Am Midl Nat 168:112–131.  https://doi.org/10.1674/0003-0031-168.1.112 CrossRefGoogle Scholar
  78. Willacker JJ Jr, Sobczak WV, Colburn EA (2009) Stream macroinvertebrate communities in paired hemlock and deciduous watersheds. Northeast Nat 16:101–112.  https://doi.org/10.1656/045.016.0108 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Schiermeier Olentangy River Wetland Research Park, School of Environment and Natural ResourcesThe Ohio State UniversityColumbusUSA
  2. 2.Department of BiologyUniversity of Nebraska at OmahaOmahaUSA

Personalised recommendations