Spring bird migration as a dispersal mechanism for the hemlock woolly adelgid

Abstract

In eastern North America, the invasive hemlock woolly adelgid (Adelges tsugae Annand), has expanded northward at a pace that exceeds predictions from mechanistic models, suggesting successful long-distance dispersal despite the only viable dispersive phase being a flightless nymph, or “crawler.” We hypothesize that migrating birds may contribute to long-distance dispersal of crawlers by passively transporting them in their plumage during northward migration. We collected hemlock woolly adelgid crawlers from the plumage of wild birds in Connecticut hemlock forests in spring and summer 2016–2017 and evaluated the factors that influence crawler loads on wild birds. Of 456 birds examined, 40 individuals of 22 species carried adelgid crawlers. Crawler loads varied strongly over time, showing a mid-spring peak that mirrored the phenological pattern in crawler abundance. However, crawler load was not affected by either local crawler abundance at capture sites or the degree of bird species association with hemlock forests. To test whether dispersed crawlers could start new invasions, we experimentally simulated avian-assisted dispersal of adelgids onto uninfested nursery hemlocks. Although rare, crawlers placed on birds did settle successfully on experimental branches during the adelgid’s summer generation. Our study confirms that birds carry hemlock woolly adelgid crawlers most often during the period of peak spring songbird migration, and that crawlers can move off bird plumage to settle on hemlock foliage. Bird-mediated, long-distance dispersal of crawlers likely has played a key role in hemlock woolly adelgid spread, and with warming temperatures, this mechanism may continue to be important for future range expansion.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Anastácio PM, Ferreira MP, Banha F, Capinha C, Rabaça JE (2013) Waterbird-mediated passive dispersal is a viable process for crayfish (Procambarus clarkii). Aquat Ecol 48:1–10

    Article  Google Scholar 

  2. Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178

    Article  Google Scholar 

  3. Bauer S, Hoye BJ (2014) Migratory animals couple biodiversity and ecosystem functioning worldwide. Science 344:1242552. https://doi.org/10.1126/science.1242552

    Article  CAS  Google Scholar 

  4. Becker DA, Brittingham MC, Goguen CB (2008) Effects of hemlock woolly adelgid on breeding birds at Fort Indiantown Gap, Pennsylvania. Northeast Nat 15:227–240. https://doi.org/10.1656/1092-6194(2008)15%5b227:EOHWAO%5d2.0.CO;2

    Article  Google Scholar 

  5. Blackman RL, Eastop VF (1994) Aphids on the world’s crops: an identification and information guide. CAB International, Wallingford

    Google Scholar 

  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Springer, New York

    Google Scholar 

  7. Butin E, Porter AH, Elkinton J (2005) Adaptation during biological invasions and the case of Adelges tsugae. Evol Ecol Res 7:887–900

    Google Scholar 

  8. Carlo TA, Morales JM (2016) Generalist birds promote tropical forest regeneration and increase plant diversity via rare-biased seed dispersal. Ecology 97:1819–1831. https://doi.org/10.1515/aiht-2015-66-25

    Article  PubMed  Google Scholar 

  9. Carlo TA, Tewksbury JJ (2013) Directness and tempo of avian seed dispersal increases emergence of wild chiltepins in desert grasslands. J Ecol 102:248–255. https://doi.org/10.1111/1365-2745.12180

    Article  Google Scholar 

  10. Carlo TA, Tewksbury JJ, del Río CM (2009) A new method to track seed dispersal and recruitment using 15 N isotope enrichment. Ecology 90:3516–3525. https://doi.org/10.1890/08-1313.1

    Article  PubMed  Google Scholar 

  11. Charalambidou I, Santamaria L (2002) Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence. Acta Oecol 23:165–176. https://doi.org/10.1016/S1146-609X(02)01148-7

    Article  Google Scholar 

  12. Charalambidou I, Santamaria L, Langevoord O (2003) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Funct Ecol 17:747–753. https://doi.org/10.1111/j.1365-2435.2003.00787.x

    Article  Google Scholar 

  13. Cheah C (2016) HWA winter mortality in Connecticut and implications for management and control. Connecticut Agricultural Experiment Station Factsheet. http://www.ct.gov/caes/lib/caes/documents/publications/fact_sheets/plant_pathology_and_ecology/hemlock_woolly_adelgid_winter_mortality__7.12.16.pdf. Accessed 13 Oct 2018

  14. Cheah CASJ (2017) Predicting hemlock woolly adelgid winter mortality in Connecticut forests by climate divisions. Northeast Nat 24:B90–B118. https://doi.org/10.1656/045.024.s713

    Article  Google Scholar 

  15. Ellison AM (2014) Experiments are revealing a foundation species: a case study of eastern hemlock (Tsuga canadensis). Adv Ecol 2014:1–11. https://doi.org/10.1126/science.1221748

    Article  CAS  Google Scholar 

  16. Emilson C, Bullas-Appleton E, McPhee D et al (2018) Hemlock woolly adelgid management plan for Canada. Natural Resources Canada, Canadian Forest Service, Sault Ste. Marie

    Google Scholar 

  17. Ferrari JR, Preisser EL, Fitzpatrick MC (2013) Modeling the spread of invasive species using dynamic network models. Biol Invasions 16:949–960. https://doi.org/10.1007/s10530-013-0552-6

    Article  Google Scholar 

  18. Fidgen JG, Whitmore MC, Turgeon JJ (2015) Detection of hemlock woolly adelgid (Hemiptera: Adelgidae) infestations with sticky traps. Great Lakes Entomol 48:125–131

    Google Scholar 

  19. Fitzpatrick MC, Preisser EL, Porter A et al (2012) Modeling range dynamics in heterogeneous landscapes: invasion of the hemlock woolly adelgid in eastern North America. Ecol Appl 22:472–486. https://doi.org/10.1890/11-0009.1

    Article  PubMed  Google Scholar 

  20. Gibbs A (2002) Regulating hemlock woolly adelgid in noninfested states. In: Onken B, Reardon R, Lashomb J (eds) Proceedings: hemlock woolly adelgid in the eastern United States symposium. Rutgers University, East Brunswick, pp 310–312

    Google Scholar 

  21. Havill NP, Shiyake S, Lamb Galloway A et al (2016) Ancient and modern colonization of North America by hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia. Mol Ecol 25:2065–2080. https://doi.org/10.1111/mec.13589

    Article  Google Scholar 

  22. Howe RW, Mossman M (1995) The significance of hemlock for breeding birds in the western Great Lakes region. In: Mroz G, Martin J (eds) Hemlock Ecology and Management. Department of Forestry, University of Wisconsin, Madison, pp 125–139

    Google Scholar 

  23. La Sorte FA, Fink D, Hochachka WM, Kelling S (2016) Convergence of broad-scale migration strategies in terrestrial birds. Proc R Soc B Biol Sci 283:20152588. https://doi.org/10.1098/rspb.2015.2588

    Article  CAS  Google Scholar 

  24. Lebedeva NV, Krivolutsky DA (2003) Birds spread soil microarthropods to Arctic islands. Dokl Biol Sci 391:329–332

    Article  CAS  PubMed  Google Scholar 

  25. Lewis LR, Rozzi R, Goffinet B (2014) Direct long-distance dispersal shapes a New World amphitropical disjunction in the dispersal-limited dung moss Tetraplodon (Bryopsida: Splachnaceae). J Biogeogr 41:2385–2395. https://doi.org/10.1111/jbi.12385

    Article  Google Scholar 

  26. Mausel DL, Salom SM, Kok LT, Fidgen JG (2008) Propagation, synchrony, and impact of introducted and native Laricobius spp. (Coleoptera: Derodontidae) on hemlock woolly adelgid in Virginia. Environ Entomol 37:1498–1507

    Article  CAS  PubMed  Google Scholar 

  27. McAvoy TJ, Régnière J, St-Amant R, Schneeberger NF, Salom SM (2017) Mortality and recovery of hemlock woolly adelgid (Adelges tsugae) in response to winter temperatures and predictions for the future. Forests 8:497. https://doi.org/10.3390/f8120497

    Article  Google Scholar 

  28. McClure MS (1987) Biology and control of hemlock woolly adelgid. Bulletin of the Connecticut Agricultural Experiment Station, New Haven

    Google Scholar 

  29. McClure MS (1989) Evidence of a polymorphic life cycle in the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae). Ann Entomol Soc Am 82:50–54. https://doi.org/10.1093/aesa/82.1.50

    Article  Google Scholar 

  30. McClure MS (1990) Role of wind, birds, deer, and humans in the dispersal of hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 19:36–43. https://doi.org/10.1093/ee/19.1.36

    Article  Google Scholar 

  31. McClure MS (1991) Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environ Entomol 20:258–264. https://doi.org/10.1093/ee/20.1.258

    Article  Google Scholar 

  32. McClure M (1992) Hemlock woolly adelgid. Am Nurseryman 176(6):82–89

    Google Scholar 

  33. McKenzie EA, Elkinton JS, Casagrande RA, Preisser EL, Mayer M (2014) Terpene chemistry of eastern hemlocks resistant to hemlock woolly adelgid. J Chem Ecol 40:1003–1012

    Article  CAS  PubMed  Google Scholar 

  34. Morin RS, Liebhold AM, Gottschalk KW (2009) Anisotropic spread of hemlock woolly adelgid in the eastern United States. Biol Invasions 11:2341–2350. https://doi.org/10.1007/s10530-008-9420-1

    Article  Google Scholar 

  35. Morin RS, Oswalt SN, Trotter RT III, Liebhold AM (2011) Status of hemlock in the eastern United States. U.S. Department of Agriculture Forest Service, e-science Update SRS-038

  36. Orwig DA, Thompson JR, Povak NA et al (2012) A foundation tree at the precipice: Tsuga canadensis health after the arrival of Adelges tsugae in central New England. Ecosphere. https://doi.org/10.1890/es11-0277.1

    Article  Google Scholar 

  37. 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 Change 13:541–554. https://doi.org/10.1007/s11027-007-9127-0

    Article  Google Scholar 

  38. Popp M, Mirré V, Brochmann C (2011) A single Mid-Pleistocene long-distance dispersal by a bird can explain the extreme bipolar disjunction in crowberries (Empetrum). Proc Natl Acad Sci USA 108:6520–6525. https://doi.org/10.1073/pnas.1012249108

    Article  PubMed  Google Scholar 

  39. Preisser EL, Lodge AG, Orwig DA, Elkinton JS (2007) Range expansion and population dynamics of co-occurring invasive herbivores. Biol Invasions 10:201–213. https://doi.org/10.1007/s10530-007-9123-z

    Article  Google Scholar 

  40. R Core Team(2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  41. Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: west nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 1:5–12. https://doi.org/10.3121/cmr.1.1.5

    Article  PubMed  PubMed Central  Google Scholar 

  42. Reynolds C, Miranda NAF, Cumming GS (2015) The role of waterbirds in the dispersal of aquatic alien and invasive species. Divers Distrib 21:744–754. https://doi.org/10.1111/ddi.12334

    Article  Google Scholar 

  43. Rohr JR, Mahan CG, Kim KC (2009) Response of arthropod biodiversity to foundation species declines: the case of the eastern hemlock. For Ecol Manag 258:1503–1510. https://doi.org/10.1016/j.foreco.2009.07.002

    Article  Google Scholar 

  44. Russo NJ, Cheah CASJ, Tingley MW (2016) Experimental evidence for branch-to-bird transfer as a mechanism for avian dispersal of the hemlock woolly adelgid (Hemiptera: Adelgidae). Environ Entomol 45:1107–1114. https://doi.org/10.1093/ee/nvw083

    Article  PubMed  Google Scholar 

  45. Sauer JR, Hines JE, Thomas I, Fallon J, Gough G (1999) The North American Breeding Bird Survey, results and analysis 19661998. Version 98.1. USGS Patuxent Wildlife Research Center, Laurel, MD. https://www.mbr-pwrc.usgs.gov/bbs/bbs98.html. Accessed 23 Oct 2018

  46. Scharf CS, DePalma NK (1981) Birds and mammals as vectors of the chestnut blight fungus (Endothia parasitica). Can J Zool 59:1647–1650

    Article  Google Scholar 

  47. 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 260:1677–1688. https://doi.org/10.1016/j.foreco.2010.08.007

    Article  Google Scholar 

  48. Stevens MI, Hogg ID (2003) Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica. Mol Ecol 12:2357–2369. https://doi.org/10.1046/j.1365-294X.2003.01907.x

    Article  CAS  PubMed  Google Scholar 

  49. Stoetzel MB (2002) History of the introduction of Adelges tsugae based on voucher specimens in the Smithsonian Institute National Collection of Insects. In: Onken B, Reardon R, Lashomb J (eds) Proceedings: hemlock woolly adelgid in the eastern United States symposium. Rutgers University, East Brunswick

    Google Scholar 

  50. Suetsugu K, Funaki S, Takahashi A et al (2018) Potential role of bird predation in the dispersal of otherwise flightless stick insects. Ecology 99:1504–1506. https://doi.org/10.1002/ecy.2230

    Article  PubMed  Google Scholar 

  51. Tingley MW, Orwig DA, Field R, Motzkin G (2002) Avian response to removal of a forest dominant: consequences of hemlock woolly adelgid infestations. J Biogeogr 29:1505–1516

    Article  Google Scholar 

  52. Tobin PC, Turcotte RM, Snider DA (2013) When one is not necessarily a lonely number: initial colonization dynamics of Adelges tsugae on eastern hemlock, Tsuga canadensis. Biol Invasions 15:1925–1932. https://doi.org/10.1007/s10530-013-0421-3

    Article  Google Scholar 

  53. Toenies MJ, Miller DAW, Marshall MR, Stauffer GE (2018) Shifts in vegetation and avian community structure following the decline of a foundational forest species, the eastern hemlock. Condor 120:489–506. https://doi.org/10.1650/CONDOR-17-204.1

    Article  Google Scholar 

  54. Turner JL, Fitzpatrick MC, Preisser EL (2011) Simulating the dispersal of hemlock woolly adelgid in the temperate forest understory. Entomol Exp Appl 141:216–223. https://doi.org/10.1111/j.1570-7458.2011.01184.x

    Article  Google Scholar 

  55. van Leeuwen CHA, van der Velde G (2012) Prerequisites for flying snails: external transport potential of aquatic snails by waterbirds. Freshw Sci 31:963–972. https://doi.org/10.1899/12-023.1

    Article  Google Scholar 

  56. Viana DS, Santamaria L, Michot TC, Figuerola J (2013) Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms. Ecography 36:430–438. https://doi.org/10.1111/j.1600-0587.2012.07588.x

    Article  Google Scholar 

  57. Viana DS, Santamaria L, Figuerola J (2016) Migratory birds as global dispersal vectors. Trends Ecol Evol 31:763–775. https://doi.org/10.1016/j.tree.2016.07.005

    Article  PubMed  Google Scholar 

  58. Wood SN (2010) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B (Stat Methodol) 73:3–36. https://doi.org/10.1111/j.1467-9868.2010.00749.x

    Article  Google Scholar 

  59. 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. https://doi.org/10.1093/aesa/88.6.827

    Article  Google Scholar 

  60. Zuckerberg B, Fink D, La Sorte FA, Hochachka WM, Kelling S (2016) Novel seasonal land cover associations for eastern North American forest birds identified through dynamic species distribution modelling. Divers Distrib 22:717–730

    Article  Google Scholar 

  61. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Google Scholar 

Download references

Acknowledgements

Funding for this research came from the University of Connecticut IDEA and SURF Grant Programs, the Wilson Ornithological Society Jed Burtt Mentoring Grant and a Great Hollow Ecological Research Grant. We thank UConn Forest, Yale-Myers Forest, the Connecticut Agricultural Experiment Station, Great Hollow Nature Preserve, and Bent of the River Audubon Sanctuary for allowing us to conduct research on their property. We also thank Carole Cheah and Emmett Varricchio for aiding in the planting and watering of nursery hemlocks used in this study, and consultation during experiments. Thank you to Robert Bagchi and members of the UConn Bird Lab group for feedback on study design, statistical methods, and an early draft of this manuscript.

Author information

Affiliations

Authors

Contributions

NJR and MWT conceived and designed the experiments. NJR performed the experiments with assistance of CSE and NPH. NJR and MWT analyzed the data. NJR wrote the first draft of the manuscript; all authors contributed to the final version.

Corresponding author

Correspondence to Morgan W. Tingley.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Russo, N.J., Elphick, C.S., Havill, N.P. et al. Spring bird migration as a dispersal mechanism for the hemlock woolly adelgid. Biol Invasions 21, 1585–1599 (2019). https://doi.org/10.1007/s10530-019-01918-w

Download citation

Keywords

  • Adelges tsugae
  • Biotic interactions
  • Phenology
  • Invasive species
  • Ectozoochory