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Modeling a cross-ecosystem subsidy: forest songbird response to emergent aquatic insects

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Abstract

Context

Resource movements across ecosystem boundaries are important determinants of the diversity and abundance of organisms in the donor and recipient ecosystem. However the effects of cross-ecosystem movements of materials at broader spatial extents than a typical field study are not well understood.

Objectives

We tested the hypotheses that (1) variation in abundance of 57 forest songbird species within four foraging guilds is explained by modeled emergent aquatic insect biomass inputs from adjacent lakes and streams and (2) the degree of association varies across foraging guilds and species within guilds. We also sought to determine the importance of emergent aquatic insects while accounting for variation in local forest cover and edge.

Methods

We spatially modeled the degree to which distribution and abundance of songbirds in different foraging guilds was explained by modeled emergent aquatic insect biomass. We used multilevel models to simultaneously estimate the responses of species in four different insectivorous guilds. Bird abundance was summarized from point counts conducted over 24 years at 317 points.

Results

Aerial insectivores were more abundant in areas with high estimated emergent insect biomass inputs to land (regression coefficient 0.30, P < 0.05) but the overall abundance of gleaners, bark-probers, and ground-foragers was not explained by estimated emergent insect abundance. The coursing aerial insectivores had the strongest association with emergent insects followed by willow flycatcher, olive-sided flycatcher, and alder flycatcher.

Conclusions

Modeling cross-ecosystem movements of materials at broad spatial extents can effectively characterize the importance of this ecological process for aerial insectivorous songbirds.

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Data availability

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

References

  • Bartrons M, Papes M, Diebel MW, Gratton C, Vander Zanden MJ (2013) Regional level inputs of emergent aquatic insects from water to land. Ecosystems 16:1353–1363

    Article  CAS  Google Scholar 

  • Bates D, Maechler M., Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7, https://CRAN.R-project.org/package=lme4

  • Beal FE (1912) Food of our important flycatchers. Biological Survey Bulletin 44:1–67

    Google Scholar 

  • Bub BR, Flaspohler DJ, Huckins CJF (2004) Riparian and upland breeding-bird assemblages along headwater streams in Michigan’s upper peninsula. J Wildl Manag 68:383–392

    Article  Google Scholar 

  • Bultman H, Hoekman D, Dreyer J, Gratton C (2014) Terrestrial deposition of aquatic insects increases plant quality for insect herbivores and herbivore density. Ecol Entomol 39:419–426

    Article  Google Scholar 

  • Burke DM, Nol E (1998) Influence of food abundance, nest-site habitat, and forest fragmentation on breeding Ovenbirds. Auk 115:96–104

    Article  Google Scholar 

  • Cummins KW, Wuycheck JC (1971) Caloric equivalents for investigations of ecological energetics. Int Assoc Theoret Appl Limnol Spec Commun 18:1–158

    Google Scholar 

  • Diggle PJ, Ribeiro PJ Jr (2007) Model based geostatistics. Springer, New York

    Book  Google Scholar 

  • Dreyer J, Hoekman D, Gratton C (2012) Lake-derived midges increase abundance of shoreline terrestrial arthropods. Oikos 121:252–258

    Article  Google Scholar 

  • Ehrlich P, Dobkin DS, Wheye D (1988) Birder’s handbook. Simon and Schuster, New York

    Google Scholar 

  • Epanchin PN, Knapp RA, Lawler SP (2010) Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. Ecology 91:2406–2415

    Article  PubMed  Google Scholar 

  • ESRI (2011) ArcGIS desktop: release 10. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Fitzpatrick JW (1980) Foraging behavior of neotropical tyrant flycatchers. Condor 82(1):43–57

    Article  Google Scholar 

  • Gelman A, Hill J (2006) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gende SM, Willson MF (2001) Passerine densities in riparian forests of southeast Alaska: potential effects of anadromous spawning salmon. Condor 103:624–629

    Article  Google Scholar 

  • Gorzo JM, Pidgeon AM, Thogmartin WE, Allstadt AJ, Radeloff VC, Heglund PJ, Vavrus SJ (2016) Using the North American Breeding Bird Survey to assess broad-scale response of the continent's most imperiled avian community, grassland birds, to weather variability. Condor 118:502–512

    Article  Google Scholar 

  • Gratton C, Donaldson J, Vander Zanden MJ (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11:764–774

    Article  Google Scholar 

  • Gratton C, Vander Zanden MJ (2009) Flux of aquatic insect productivity to land: comparison of lentic and lotic ecosystems. Ecology 90:2689–2699

    Article  PubMed  Google Scholar 

  • Gray LJ (1993) Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am Midl Nat 129:288–300

    Article  Google Scholar 

  • Harrison XA (2014) Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2:e616

    Article  PubMed  PubMed Central  Google Scholar 

  • Henschel JR, Mahsberg D, Stumpf H (2001) Allochthonous aquatic insects increase predation and decrease herbivory in river shore food webs. Oikos 93:429–438

    Article  Google Scholar 

  • Hoekman D, Bartrons M, Gratton C (2012) Ecosystem linkages revealed by experimental lake-derived isotope signal in heathland food webs. Oceologia 170:735–743

    Article  Google Scholar 

  • Holmes RT, Black CP, Sherry TW (1979) Comparative population bioenergetics of three insectivorous passerines in a deciduous forest. Condor 81:9–20

    Article  Google Scholar 

  • Holmes RT, Schultz JC (1988) Food availability for forest birds: effects of prey distribution and abundance on bird foraging. Can J Zool 66:720–728

    Article  Google Scholar 

  • Homer C, Dewitz J, Fry J, Coan M, Hossain N, Larson C, Herold N, McKerrow A, VanDriel JN, Wickham J (2007) Completion of the 2001 national land cover database for conterminous United States. Photogramm Eng Remote Sens 73:337–341

    Google Scholar 

  • Howe RW, Roberts LJ (2006) Sixteen years of habitat-based bird monitoring in the Nicolet National Forest. In: Ralph CJ, Rich TD (eds) Bird conservation implementation and integration in the Americas, General Technical Report PSW-GTR-191. US Department of Agriculture, Forest Service, Albany, pp 963–973

    Google Scholar 

  • Howe RW, Wolf AT, Rinaldi T (1995) Monitoring birds in a regional landscape: lessons from the Nicolet National Forest Bird Survey. USDA Forest Service Gen. Tech. Rep. PSW-GTR-149

  • Ives AR, Einarsson Á, Jansen VA, Gardarsson A (2008) High-amplitude fluctuations and alternative dynamical states of midges in Lake Myvatn. Nature 452:84–87

    Article  CAS  PubMed  Google Scholar 

  • Iwata T, Nakano S, Murakami M (2003) Stream meanders increase insectivorous bird abundance in riparian deciduous forests. Ecography 26:325–337

    Article  Google Scholar 

  • Jackson MM, Turner MG, Pearson SM, Ives AR (2012) Seeing the forest and the trees: multilevel models reveal both species and community patterns. Ecosphere 3:1–16

    Article  Google Scholar 

  • Kennedy CH (1950) The relation of American dragonfly-eating birds to their prey. Ecol Monogr 20:103–142

    Article  Google Scholar 

  • Knight TM, McCoy MW, Chase JM, McCoy KA, Holt RD (2005) Trophic cascades across ecosystems. Nature 437:880–883

    Article  CAS  PubMed  Google Scholar 

  • Kristan WB III, Johnson MD, Rotenberry JT (2007) Choices and consequences of habitat selection for birds. Condor 109:485–488

    Article  Google Scholar 

  • Lindsay AR, Gillum SS, Meyer MW (2002) Influence of lakeshore development on breeding bird communities in a mixed northern forest. Biol Conserv 107:1–11

    Article  Google Scholar 

  • MacArthur RH (1958) Population ecology of some warblers of northeastern coniferous forests. Ecology 39:599–619

    Article  Google Scholar 

  • Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88(1):140–148

    Article  PubMed  Google Scholar 

  • McCollin D (1998) Forest edges and habitat selection in birds: a functional approach. Ecography 21(3):247–260

    Article  Google Scholar 

  • McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Computer software program produced by the authors at the University of Massachusetts, Amherst. https://www.umass.edu/landeco/research/fragstats/fragstats.html

  • Morse DH (1989) American warblers: an ecological and behavioral perspective. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nebel S, Mills A, McCraken J, Taylor PD (2010) Declines of aerial insectivores in North America follow a geographic gradient. Avian Conserv Ecol 5:1

    Article  Google Scholar 

  • Niemi GJ, Howe RW, Sturtevant BR, Parker LR, Grinde AR, Danz NP, Nelson MD, Zlonis EJ, Walton NG, Giese EEG and Lietz SM (2016) Analysis of long-term forest bird monitoring data from national forests of the western Great Lakes Region. Gen. Tech. Rep. NRS-159. Newtown Square, PA: US Department of Agriculture, Forest Service, Northern Research Station, pp 1–322

  • Pickett ST, Cadenasso ML (1995) Landscape ecology: spatial heterogeneity in ecological systems. Science 269(5222):331–334

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Polis GA, Hurd SD (1995) Extraordinarily high spider densities on islands: flow of energy from the marine to terrestrial food webs and the absence of predation. Proc Natl Acad Sci USA 92:4382–4386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ribeiro PJ Jr, Diggle PJ (2001) geoR: a package for geostatistical analysis. R-NEWS 1(2):15–18

    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 

  • Sabo JL, Power ME (2002) River–watershed exchange: effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1860–1869

    Google Scholar 

  • Sherry TW (1979) Competitive interactions and adaptive strategies of American Redstarts and Least Flycatchers in a northern hardwoods forest. Auk 96:265–283

    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 

  • Van Wilgenburg SL, Mazerolle DF, Hobson KA (2001) Patterns of arthropod abundance, vegetation, and microclimate at boreal forest edge and interior in two landscapes: implications for forest birds. Ecoscience 8(4):454–461

    Article  Google Scholar 

  • Vander Zanden MJ, Gratton C (2011) Blowin' in the wind: reciprocal airborne carbon fluxes between lakes and land. Can J Fish Aquat Sci 68:170–182

    Article  CAS  Google Scholar 

  • Veech JA, Pardieck KL, Ziolkowski DJ Jr (2017) How well do route survey areas represent landscapes at larger spatial extents? An analysis of land cover composition along Breeding Bird Survey routes. Condor 119(3):607–615

    Article  Google Scholar 

  • WDNR (2011) Online document. https://dnr.wi.gov/maps/gis/datahydro.html. Madison, WI.

  • Whitaker DM, Carroll AL, Montevecchi WA (2000) Elevated numbers of flying insects and insectivorous birds in riparian buffer strips. Can J Zool 78:740–747

    Article  Google Scholar 

  • Whitaker DM, Montevecchi WA (1997) Breeding bird assemblages associated with riparian, interior forest, and nonriparian edge habitats in a balsam fir ecosystem. Can J For Res 27(8):1159–1167

    Article  Google Scholar 

  • Wolf AT, Howe RW, Davis GJ (1995) Detectability of forest birds from stationary points in northern Wisconsin. In: Ralph CJ, Sauer JR, Droege S (eds) Monitoring bird populations by point counts. Gen. Tech. Rep. PSW-GTR-149, vol 149. US Department of Agriculture, Forest Service, Pacific Southwest Research Station, Albany, pp 19–24

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Acknowledgements

PS was supported by a NSF Graduate Research Fellowship. MB, JVZ, and CG were supported by National Science Foundation Grants DEB-0717148, DEB-LTREB-1052160, and DEB-LTREB-1556208. We thank A.R. Ives who provided valuable suggestions that improved the analysis, the many Nicolet National Forest Bird Survey volunteers who gathered the bird count data over 24 years, and the Department of Forest and Wildlife Ecology, UW-Madison, for support.

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Authors and Affiliations

  1. SILVIS Lab, Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI, 53706, USA

    Paul R. Schilke & Anna M. Pidgeon

  2. Aquatic Ecology Group, University of Vic - Central University of Catalonia, Vic, Catalonia, Spain

    Mireia Bartrons

  3. Natural Resources Research Institute, University of Minnesota-Duluth, 5013 Miller Trunk Hwy, Hermantown, MN, 55811, USA

    Jessica M. Gorzo

  4. Center for Limnology, University of Wisconsin-Madison, 680 N Park St, Madison, WI, 53706, USA

    M. Jake Vander Zanden

  5. Department of Entomology, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI, 53706, USA

    Claudio Gratton

  6. Cofrin Center for Biodiversity, University of Wisconsin-Green Bay, 2420 Nicolet Drive, Green Bay, WI, 54311, USA

    Robert W. Howe

Authors
  1. Paul R. Schilke
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  2. Mireia Bartrons
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  6. Robert W. Howe
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Contributions

PS analyzed the data and wrote the paper. MB, JVZ, and CG conceived the idea and assisted with writing the paper. JG assisted with data analysis and interpretation of results and assisted with writing the paper. RH contributed the bird data and assisted with writing the paper. AP assisted with the idea, analysis, and writing.

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Correspondence to Paul R. Schilke.

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Schilke, P.R., Bartrons, M., Gorzo, J.M. et al. Modeling a cross-ecosystem subsidy: forest songbird response to emergent aquatic insects. Landscape Ecol 35, 1587–1604 (2020). https://doi.org/10.1007/s10980-020-01038-0

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