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Indirect effects of an invasive exotic species on a long-distance migratory songbird

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Abstract

The loss of foundational tree species to non-native pests can have far reaching consequences for forest composition and function, yet little is known about the impacts on other ecosystem components such as wildlife. We had the opportunity to observe how the loss of eastern hemlock (Tsuga canadensis), due to the invasive hemlock woolly adelgid (Adelges tsugae), influenced the population ecology of the Black-throated Blue Warbler (Setophaga caerulescens) over a 7 year period. We followed the process of adelgid infestation and subsequent hemlock loss, which allowed us to investigate the patterns and mechanisms of population change. We document a precipitous decline in breeding pairs at one site where hemlock was most abundant in the understory, but not at our other two sites. We observed no changes in reproductive output or apparent survival, yet territory size increased dramatically at the most affected site, suggesting that the decline was due to a lack of colonization by new breeders. Our results demonstrate how an invasive insect pest can indirectly influence wildlife species not believed to be vulnerable and in ways not typically investigated.

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References

  • Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest

    Google Scholar 

  • Allen MC, Sheehan J, Master TL, Mulvihill R (2009) Responses of Acadian Flycatchers (Empidonax virescens) to hemlock woolly adelgid (Adelges tsugae) infestation in Appalachian riparian forests. Auk 126:543–553

    Article  Google Scholar 

  • Bayne EM, Hobson KA (2002) Apparent survival of male ovenbirds in fragmented and forested boreal landscapes. Ecology 83:1307–1316

    Google Scholar 

  • Becker DA, Brittingham MC, Goguen CB (2008) Effects of hemlock woolly adelgid on breeding birds at Fort Indiantown Gap, Pennsylvania. Northeastern Naturalist 15:227–240

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science, New York

    Google Scholar 

  • Castello JD, Leopold DJ, Smallidge PJ (1995) Pathogens, patterns, and processes in forest ecosystems. Bioscience 45:16–24

    Article  Google Scholar 

  • Day FPJ, Monk CD (1974) Vegetation patterns on a southern Appalachian watershed. Ecology 55:1064–1074

    Article  Google Scholar 

  • Day FPJ, Phillips DL, Monk CD (1988) Forest communities and patterns. In: Swank WT, Crossley DAJ (eds) Forest hydrology and ecology at Coweeta, ecological studies 66. Springer, New York

    Google Scholar 

  • Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliot 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, Holle BV, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Article  Google Scholar 

  • Enserink M (1999) Biological invaders sweep in. Science 285:1834–1836

    Article  CAS  Google Scholar 

  • Eschtruth AK, Cleavitt NL, Battles JJ, Evans RA, Fahey TJ (2006) Vegetation dynamics in declining eastern hemlock stands: 9 years of forest response to hemlock woolly adelgid infestation. Can J For Res-Revue Canadienne De Recherche Forestiere 36:1435–1450

    Article  Google Scholar 

  • Everett RA (2000) Patterns and pathways of biological invasions. Trends Ecol Evol 15:177–178

    Article  Google Scholar 

  • Farnsworth GL, Simons TR (2001) How many baskets? Clutch sizes that maximize annual fecundity of multiple-brooded birds. Auk 118:973–982

    Google Scholar 

  • Farnsworth GL, Simons TR (2005) Relationship between Mayfield nest-survival estimates and seasonal fecundity: a cautionary reply. Auk 122:1000–1001

    Article  Google Scholar 

  • Gandhi KJK, Herms DA (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405

    Article  Google Scholar 

  • Gerrard PD, Smith DR, Weerakkody G (1998) Limits of retrospective power analysis. J Wildl Manag 62:801–807

    Google Scholar 

  • Goodbred CO, Holmes RT (1996) Factors affecting food provisioning of nestling Black-throated Blue Warblers. Wilson Bull 108:467–479

    Google Scholar 

  • Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21

    Article  Google Scholar 

  • Herkert JR, Reinking DL, Wiedenfeld DA, et al (2003) Effects of prairie fragmentation on the nest success of breeding birds in the midcontinental United States. Conserv Biol 17:587–594

    Google Scholar 

  • Holmes RT, Sherry TW, Marra PP, Petit KE (1992) Multiple brooding and productivity of a neotropical migrant, the Black-throated Blue Warbler (Dendroica caerulescens), in an unfragmented temperate forest. Auk 109:321–333

    Article  Google Scholar 

  • Holmes RT, Marra PP, Sherry TW (1996) Habitat specific demography of breeding black-throated blue warblers (Dendroica caerulescens): implications for population dynamics. J Anim Ecol 65:183–195

    Article  Google Scholar 

  • Holmes RT, Rodenhouse NL, Sillett TS (2005) Black-throated Blue Warbler (Dendroica caerulescens). In: Poole A (ed) The birds of North America. Cornell Lab of Ornithology; Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/087doi:bna.87, Ithaca, NY, USA

  • Hoover JP (2003) Decision rules for site fidelity in a migratory bird, the prothonotary warbler. Ecology 84:416–430

    Article  Google Scholar 

  • Hosmer DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

    Google Scholar 

  • James FC (1971) Ordinations of habitat relationships among breeding birds. Wilson Bull 83:215–236

    Google Scholar 

  • Johnson DH (1999) The insignificance of statistical significance testing. J Wildl Manag 63:763–772

    Google Scholar 

  • Jones J, Doran PJ, Nagy LR, Holmes RT (2005a) Mayfield nest-survival estimates and seasonal fecundity: reply to Farnsworth and Simons. Auk 122:1001–1003

    Article  Google Scholar 

  • Jones J, Doran PJ, Nagy LR, Holmes RT (2005b) Relationship between Mayfield nest-survival estimates and seasonal fecundity: a cautionary note. Auk 122:306–312

    Article  Google Scholar 

  • Kincaid JA, Parker AJ (2008) Structural characteristics and canopy dynamics of Tsuga canadensis in forests of the southern Appalachian Mountains, USA. Plant Ecol 199:265–280

    Article  Google Scholar 

  • Kizlinski ML, Orwig DA, Cobb RC, Foster DR (2002) Direct and indirect ecosystem consequences of an invasive pest on forests dominated by eastern hemlock. J Biogeogr 29:1489–1503

    Article  Google Scholar 

  • Lebreton JD, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

    Article  Google Scholar 

  • Liebhold AM, Macdonald WL, Bergdahl D, et al (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci 41:1–49

    Google Scholar 

  • Loo J (2009) Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol Invasions 11:81–96

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Google Scholar 

  • Manolis JC, Anderson DE, Cuthbert FJ (2000) Uncertain nest fates in songbird studies and variation in Mayfield estimation. Auk 117:615–626

    Google Scholar 

  • Marshall MR, Cooper RJ (2004) Territory size of a migratory songbird in response to caterpillar density and foliage structure. Ecology 85:432–445

    Article  Google Scholar 

  • Marshall MR, Cooper RJ, DeCecco JA, Stranzanac J, Butler L (2002) Effects of experimentally reduced prey abundance on the Red-eyed vireo. Ecol Appl 12:261–280

    Article  Google Scholar 

  • McClure MS (1991) Density-dependent feedback and population-cycles in Adelges tsugae (Homoptera, Adelgidae) on Tsuga canadensis. Environ Entomol 20:258–264

    Google Scholar 

  • Myers JP, Conners PG, Pitelka FA (1979) Territory size in wintering Sanderlings: the effects of prey abundance and intruder density. Auk 96:551–561

    Google Scholar 

  • Noble GK (1939) The role of dominance in the social life of birds. Auk 56:263–273

    Article  Google Scholar 

  • Novacek MJ, Cleland EE (2001) The current biodiversity extinction event: scenarios for mitigation and recovery. Proc Natl Acad Sci USA 98:5466–5470

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Orwig DA (2002) Ecosystem to regional impacts of introduced pests and pathogens: historical context, questions and issues. J Biogeogr 29:1471–1474

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Orwig DA, Foster DR, Mausel DL (2002) Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J Biogeogr 29:1475–1487

    Article  Google Scholar 

  • Pimental D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Porneluzi PA (2003) Prior breeding success affects return rates of territorial male Ovenbirds. Condor 105:73–79

    Article  Google Scholar 

  • Pulliam HR, Danielson BJ (1991) Sources, sinks, and habitat selection: a landscape perspective on population dynamics. Am Nat 137:S50–S66

    Article  Google Scholar 

  • Pyle P, Howell SNG, Yunick RP, DeSante DR (1987) Indentification guide to North American Passerines. Slate Creek Press, Bolinas

    Google Scholar 

  • Robinson SK, Holmes RT (1982) Foraging behavior of forest birds: the relationships among search tactics, diet, and habitat structure. Ecology 63:1918–1931

    Article  Google Scholar 

  • Robinson SK, Thompson FR, Donovan TM, et al (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990

    Google Scholar 

  • Rodenhouse NL, Holmes RT (1992) Results of experimental and natural food reductions for breeding Black-throated blue warblers. Ecology 73:357–372

    Article  Google Scholar 

  • Rodenhouse NL, Sillett TS, Doran PJ, Holmes RT (2003) Multiple density-dependence mechanisms regulate a migratory bird population during the breeding season. Proc R Soc Lond B 270:21105–22110

    Article  Google Scholar 

  • Rogers RS (1978) Forests dominated by hemlock (Tsuga canadensis): distribution as related to site and post-settlement history. Can J Bot 56:843–854

    Article  Google Scholar 

  • Ross RM, Bennett RM, Snyder CD, Young JA, Smith DR, Lemarie DP (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

    Article  Google Scholar 

  • Ross RM, Redell LA, Bennett RM, Young JA (2004) Mesohabitat use of threatened hemlock forests by breeding birds of the Delaware river basin in northeastern United States. Nat Areas J 24:307–315

    Google Scholar 

  • Runge JP, Runge MC, Nichols JD (2006) The role of local populations within a landscape context: defining and classifying sources and sinks. Am Nat 167:925–938

    Article  PubMed  Google Scholar 

  • SAS Institute (2007) SAS 9.1.3 Help and documentation. Cary, NC

  • Sedgwick JA (2004) Site fidelity, territory fidelity, and natal philopatry in willow flycatchers (Empidonax traillii). Auk 121:1103–1121

    Google Scholar 

  • Shaffer TL (2004) A unified approach to analyzing nest success. Auk 121:526–540

    Google Scholar 

  • Sillett TS, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. J Anim Ecol 71:296–308

    Article  Google Scholar 

  • Sillett TS, Rodenhouse NL, Holmes RT (2004) Experimentally reducing neighbor density affects reproduction and behavior of a migratory songbird. Ecology 85:2467–2477

    Article  Google Scholar 

  • Smith TM, Shugart HH (1987) Territory size variation in the Ovenbird: the role of habitat structure. Ecology 68:695–704

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Spaulding HL, Rieske LK (2010) The aftermath of an invasion: structure and composition of Central Appalachian hemlock forests following establishment of the hemlock woolly adelgid, Adelges tsugae. Biol Invasions 12:3135–3143

    Article  Google Scholar 

  • Steele BB (1992) Habitat selection by breeding Black-throated Blue Warblers at two spatial scales. Ornis Scandinavica 23:33–42

    Article  Google Scholar 

  • Steele BB (1993) Selection of foraging and nesting sites by Black-throated Blue Warblers: their relative influence on habitat choice. Condor 95:568–579

    Article  Google Scholar 

  • 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 

  • Tooley PW, Browning M (2009) Susceptibility to Phytophthora ramorum and inoculum production potential of some common eastern forest understory plant species. Plant Dis 93:249–256

    Article  Google Scholar 

  • USFS (2009) http://www.na.fs.fed.us/fhp/hwa/infestations/hwa_infestations09.pdf

  • Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Ward MP (2005) The role of immigration in the decline of an isolated migratory bird population. Conserv Biol 19:1528–1536

    Article  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Supplement):120–138

    Article  Google Scholar 

  • Wilkin TA, Garant D, Gosler AG, Sheldon BC (2006) Density effects on life-history traits in a wild population of the great tit Parus major: analyses of long-term data with GIS techniques. J Anim Ecol 75:604–615

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dave Buehler, Dan Kim, and Kay Franzreb for their assistance during the early years of this project. The Coweeta hydrology lab provided access to one of our field sites. Funding for this project was provided in part by the USFS, NSF, and the Georgia Ornithological Society. Finally, numerous field assistants made the project possible, most notably Brett Maley, Karen Leavelle, Anika Mahoney, and Liz Willenbring whose dedication over multiple field seasons was invaluable.

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Authors and Affiliations

  1. Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, 61801, USA

    Kirk W. Stodola

  2. Department of Zoology, University of Wisconsin, Madison, WI, 53706, USA

    Eric T. Linder

  3. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA, 30602, USA

    Robert J. Cooper

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  1. Kirk W. Stodola
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  2. Eric T. Linder
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  3. Robert J. Cooper
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Correspondence to Kirk W. Stodola.

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Stodola, K.W., Linder, E.T. & Cooper, R.J. Indirect effects of an invasive exotic species on a long-distance migratory songbird. Biol Invasions 15, 1947–1959 (2013). https://doi.org/10.1007/s10530-013-0423-1

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