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Landscape-scale effects of forest degradation on insectivorous birds and invertebrates in austral temperate forests

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Abstract

Context

Insectivorous birds are sensitive to forest disturbances that may limit the availability of food consisting mainly of invertebrates. However, birds and invertebrates may be differently affected by forest disturbances while invertebrates may interact with disturbances.

Objectives

We aim to determine: (i) the effects of forest degradation on invertebrates and insectivorous birds; (ii) the effect of the availability of invertebrates as a food source on birds; (iii) interactions between food availability and forest degradation.

Methods

We selected 34 1-km radius landscape units, where the abundance of birds and invertebrates was sampled in the canopy and understory. Bird density as well as the abundance and richness of invertebrates were considered as dependent variables and analysed using Generalized Linear Mixed Model and Structural Equation Models. Remote-sensing indices of forest degradation were included as predictors.

Results

Eight indices of forest degradation affected canopy and understory invertebrates differently. Unlike invertebrates, bird abundance was affected by a smaller number of degradation indices, forest amounts as well as the cover of understory and canopy. Only two forest degradation indices had a comparable effect on bird abundance and invertebrates. We found causal relationships between understory invertebrates and the abundance of understory birds (all species and the small-sized ones), but also invertebrate abundance × forest cover interactions affected the abundance of a bird species.

Conclusions

Our results indicate that birds and invertebrates respond differently to forest degradation, but also provide evidence for bottom-up control by forest degradation and suggest food limitation varies with forest amounts.

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References

  • Anjos LD (2006) Bird species sensitivity in a fragmented landscape of the Atlantic forest in southern Brazil. Biotropica 38:229–234

    Google Scholar 

  • Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Dobbs C (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B 281(1780):20133330

    PubMed  Google Scholar 

  • Bahamondez C, Thompson ID (2016) Determining forest degradation, ecosystem state and resilience using a standard stand stocking measurement diagram: theory into practice. Forestry 89:290–300

    Google Scholar 

  • Barnagaud JY, Devictor V, Jiguet F, Barbet-Massin M, Le Viol I, Archaux F (2012) Relating habitat and climatic niches in birds. PLoS ONE 7(3):e32819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattarai BP, Kindlmann P (2018) Human disturbance is the major determinant of the habitat and prey preference of the Bengal tiger (Panthera tigris tigris) in the Chitwan National Park Nepal. Eur J Ecol 4:13–21

    Google Scholar 

  • Boscolo D, Metzger JP (2009) Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales? Landsc Ecol 24:907–918

    Google Scholar 

  • Bowler DE, Heldbjerg H, Fox AD, de Jong M, Böhning-Gaese K (2019) Long-term declines of European insectivorous bird populations and potential causes. Conserv Biol 33:1120–1130

    PubMed  Google Scholar 

  • Bravo SP, Cueto VR, Gorosito CA (2017) Migratory timing, rate, routes and wintering areas of White-crested Elaenia (Elaenia albiceps chilensis), a key seed disperser for Patagonian forest regeneration. PLoS ONE 12(2)e0170188

    PubMed  PubMed Central  Google Scholar 

  • Brown D., Sherry TW (2006) Food supply controls the body condition of a migrant bird wintering in the tropics. Oecologia 149:22–32

    PubMed  Google Scholar 

  • Buckland ST, Anderson DR, Burnham KP, Laake JL (1993) Distance sampling: estimating abundance of biological populations. Chapman and Hall, London

    Google Scholar 

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

    Google Scholar 

  • Carvajal MA, Alaniz AJ, Smith-Ramírez C, Sieving KE (2018) Assessing habitat loss and fragmentation and their effects on population viability of forest specialist birds: Linking biogeographical and population approaches. Divers Distrib 24:820–830

    Google Scholar 

  • Castellon TD, Sieving KE (2007) Patch network criteria for dispersal-limited endemic birds of south american temperate rain forest. Ecol Appl 17:2152–2163

    PubMed  Google Scholar 

  • Chan EK, Yu YT, Zhang Y, Dudgeon D (2008) Distribution patterns of birds and insect prey in a tropical riparian forest. Biotropica 40:623–629

    Google Scholar 

  • Cockle KL, Areta JI (2013) Specialization on bamboo by neotropical birds. Condor 115:217–220

    Google Scholar 

  • CONAF (2011) Catastro de Los Recursos Vegetacionales Nativos de Chile: Monitoreo de Cambios Y Actualizaciones, Periodo 1997–2011.

  • Cornell KL, Donovan TM (2010) Effects of spatial habitat heterogeneity on habitat selection and annual fecundity for a migratory forest songbird. Landsc Ecol 25:109–122

    Google Scholar 

  • Díaz IA, Armesto JJ, Willson MF (2006) Mating success of the endemic Des Murs’ Wiretail (Sylviorthorhynchus desmursii, Furnariidae) in fragmented Chilean rainforests. Austral Ecol 31:13–21

    Google Scholar 

  • Díaz IA, Armesto JJ, Reid S, Sieving KE, Willson MF (2005) Linking forest structure and composition: avian diversity in successional forests of Chiloé Island, Chile. Biol Cons 123:91–101

    Google Scholar 

  • Estades CF (1997) Bird-habitat relationships in a vegetational gradient in the Andes of central Chile. The Condor 99:719–727

    Google Scholar 

  • Gonzalez-Gomez PL, Estades CF, Simonetti JA (2006) Strengthened insectivory in a temperate fragmented forest. Oecologia 148:137–143

    PubMed  Google Scholar 

  • Gorelick N, Hancher M, Dixon M, Ilyushchenko S, Thau D, Moore R (2017) Google earth engine: planetary-scale geospatial analysis for everyone. Remote Sens Environ 202:18–27

    Google Scholar 

  • Gruner DS (2004) Attenuation of top-down and bottom-up forces in a complex terrestrial community. Ecology 85:3010–3022

    Google Scholar 

  • Hallmann CA, Foppen RP, van Turnhout CA, de Kroon H, Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341–343

    CAS  PubMed  Google Scholar 

  • Hamer KC, Newton RJ, Edwards FA, Benedick S, Bottrell SH, Edwards DP (2015) Impacts of selective logging on insectivorous birds in Borneo: the importance of trophic position, body size and foraging height. Biol Cons 188:82–88

    Google Scholar 

  • Hart JD, Milsom TP, Fisher G, Wilkins V, Moreby SJ, Murray AWA, Robertson PA (2006) The relationship between yellowhammer breeding performance, arthropod abundance and insecticide applications on arable farmland. J Appl Ecol 43:81–91

    CAS  Google Scholar 

  • Hermes C, Döpper A, Schaefer HM, Segelbacher G (2016) Effects of forest fragmentation on the morphological and genetic structure of a dispersal-limited, endangered bird species. Nat Conserv 16:39

    Google Scholar 

  • Holt R, Lawton J, Polis G, Martinez N (1999) Trophic rank and the species–area relationship. Ecology 80:1495–1504

    Google Scholar 

  • Ibarra JT, Gálvez N, Altamirano TA, Caviedes J, Rojas IM, Bonacic C, Martin K (2017) Seasonal dynamics of avian guilds inside and outside core protected areas in an Andean Biosphere Reserve of southern Chile. Bird Study 64:410–420

    Google Scholar 

  • Jaksic FM, Feinsinger P (1991) Bird assemblages in temperate forests of North and South America: a comparison of diversity, dynamics, guild structure, and resource use. Revista Chilena de Historia Natural 64:491–510

    Google Scholar 

  • Johnson MD, Sherry TW (2001) Effects of food availability on the distribution of migratory warblers among habitats in Jamaica. J Anim Ecol 70:546–560

    Google Scholar 

  • Karr JR, Brawn JD (1990) Food resources of understory birds in central Panama: quantification and effects on avian populations. Stud Avian Biol 13:58–64

    Google Scholar 

  • Kéry M, Royle JA (2015) Applied hierarchical modeling in ecology: analysis of distribution, abundance and species richness in R and BUGS: Volume 1: prelude and static models. First edition. Academic Press, Amsterdam

  • Larsen S, Sorace A, Mancini L (2010) Riparian bird communities as indicators of human impacts along Mediterranean streams. Environ Manage 45:261–273

    PubMed  Google Scholar 

  • Leal AI, Acácio M, Meyer CF, Rainho A, Palmeirim JM (2019) Grazing improves habitat suitability for many ground foraging birds in Mediterranean wooded grasslands. Agr Ecosyst Environ 270:1–8

    Google Scholar 

  • Lefcheck JS (2015) piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579

    Google Scholar 

  • Lister BC, Garcia A (2018) Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc Natl Acad Sci 115(44):E10397–E10406

    CAS  PubMed  Google Scholar 

  • Luebert F, Pliscoff P (2006) Sinopsis bioclimática y vegetacional de Chile. Editorial Universitaria, Santiago

    Google Scholar 

  • Maas B, Karp DS, Bumrungsri S, Darras K, Gonthier D, Huang JCC, Morrison EB (2016) Bird and bat predation services in tropical forests and agroforestry landscapes. Biol Rev 91:1081–1101

    PubMed  Google Scholar 

  • Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127

    Google Scholar 

  • McWethy DB, Hansen AJ, Verschuyl JP (2010) Bird response to disturbance varies with forest productivity in the northwestern United States. Landsc Ecol 25:533–549

    Google Scholar 

  • Mäntylä E, Klemola T, Laaksonen T (2011) Birds help plants: a meta-analysis of top-down trophic cascades caused by avian predators. Oecologia 165:143–151

    PubMed  Google Scholar 

  • Mazia N, Chaneton EJ, Dellacanonica C, Dipaolo L, Kitzberger T (2012) Seasonal patterns of herbivory, leaf traits and productivity consumption in dry and wet Patagonian forests. Ecol Entomol 37:193–203

    Google Scholar 

  • Morante-Filho JC, Arroyo-Rodríguez V, Lohbeck M, Tscharntke T, Faria D (2016) Tropical forest loss and its multitrophic effects on insect herbivory. Ecology 97:3315–3325

    PubMed  Google Scholar 

  • Moorman CE, Bowen LT, Kilgo JC, Hanula JL, Horn S, Ulyshen MD (2012) Arthropod abundance and seasonal bird use of bottomland forest harvest gaps. Wilson J Ornithol 124:31–39

    Google Scholar 

  • Mulwa RK, Neuschulz EL, Böhning-Gaese K, Schleuning M (2013) Seasonal fluctuations of resource abundance and avian feeding guilds across forest: farmland boundaries in tropical Africa. Oikos 122:524–532

    Google Scholar 

  • O'Dea N, Whittaker RE (2007) How resilient are Andean montane forest bird communities to habitat degradation? Biodiv Conserv 16:1131–1159

    Google Scholar 

  • Perry KI, Herms DA (2017) Responses of ground-dwelling invertebrates to gap formation and accumulation of woody debris from invasive species, wind, and salvage logging. Forests 8:1–13

    CAS  Google Scholar 

  • Peter F, Berens DG, Grieve GR, Farwig N (2015) Forest fragmentation drives the loss of insectivorous birds and an associated increase in herbivory. Biotropica 47:626–635

    Google Scholar 

  • Pollock HS, Cheviron ZA, Agin TJ, Brawn JD (2015) Absence of microclimate selectivity in insectivorous birds of the Neotropical forest understory. Biol Cons 188:116–125

    Google Scholar 

  • Poulin JF, Villard MA (2011) Edge effect and matrix influence on the nest survival of an old forest specialist, the Brown Creeper (Certhia americana). Landsc Ecol 26:911–922

    Google Scholar 

  • Pöysä H, Pöysä S (2002) Nest-site limitation and density dependence of reproductive output in the common goldeneye Bucephala clangula: implications for the management of cavity-nesting birds. J Appl Ecol 39:502–510

    Google Scholar 

  • Pyke GH (1985) Seasonal patterns of abundance of insectivorous birds and flying insects. Emu 85:34–39

    Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Razeng E, Watson DM (2015) Nutritional composition of the preferred prey of insectivorous birds: popularity reflects quality. J Avian Biol 46:89–96

    Google Scholar 

  • Reid S, Díaz IA, Armesto JJ, Willson MF (2004) Importance of native bamboo for understory birds in Chilean temperate forests. Auk 121:515–525

    Google Scholar 

  • Rioux Paquette S, Pelletier F, Garant D, Bélisle M (2014) Severe recent decrease of adult body mass in a declining insectivorous bird population. Proc R Soc B 281(1786):20140649

    PubMed  Google Scholar 

  • Royle JA (2004) N-mixture models for estimating population size from spatially replicated counts. Biometrics 60:108–115

    PubMed  Google Scholar 

  • Sekercioglu CH, Ehrlich PR, Daily GC, Aygen D, Goehring D, Sandí RF (2002) Disappearance of insectivorous birds from tropical forest fragments. Proc Natl Acad Sci 99:263–267

    CAS  PubMed  Google Scholar 

  • Shipley B (2013) The AIC model selection method applied to path analytic models compared using ad-separation test. Ecology 94:560–564

    PubMed  Google Scholar 

  • Smith AC, Hudson MAR, Downes CM, Francis CM (2015) Change points in the population trends of aerial-insectivorous birds in North America: synchronized in time across species and regions. PLoS ONE 10(7):e0130768

    PubMed  PubMed Central  Google Scholar 

  • Soulé ME, Estes JA, Berger J, Del Rio CM (2003) Ecological effectiveness: conservation goals for interactive species. Conserv Biol 17:1238–1250

    Google Scholar 

  • Stanton RL, Morrissey CA, Clark RG (2018) Analysis of trends and agricultural drivers of farmland bird declines in North America: a review. Agr Ecosyst Environ 254:244–254

    Google Scholar 

  • Strong AM, Sherry TW (2000) Habitat-specific effects of food abundance on the condition of ovenbirds wintering in Jamaica. J Anim Ecol 69:883–895

    Google Scholar 

  • Thomas JA (2016) Butterfly communities under threat. Science 353:216–218

    CAS  PubMed  Google Scholar 

  • Vafidis JO, Vaughan IP, Jones TH, Facey RJ, Parry R, Thomas RJ (2016) The effects of supplementary food on the breeding performance of Eurasian reed warblers Acrocephalus scirpaceus; Implications for climate change impacts. PLoS ONE 11(7):e0159933

    PubMed  PubMed Central  Google Scholar 

  • Vergara PM (2011) Matrix-dependent corridor effectiveness and the abundance of forest birds in fragmented landscapes. Landsc Ecol 26:1085–1096

    Google Scholar 

  • Vergara PM, Simonetti JA (2004) Does nest-site cover reduce nest predation for rhinocryptids? J Field Ornithol 75:188–191

    Google Scholar 

  • Vergara PM, Simonetti JA (2006) Abundance and movement of understory birds in a Maulino forest fragmented by pine plantations. Biodivers Conserv 15:3937–3947

    Google Scholar 

  • Vergara PM, Schlatter RP (2006) Aggregate retention in two Tierra del Fuego Nothofagus forests: short-term effects on bird abundance. For Ecol Manage 225:213–224

    Google Scholar 

  • Vergara PM, Armesto JJ (2009) Responses of Chilean forest birds to anthropogenic habitat fragmentation across spatial scales. Landsc Ecol 24:25–38

    Google Scholar 

  • Vergara PM, Jiménez JE, Schlatter RP (2010) Effective point-count duration for estimating bird species’ richness in Chilean forests. Zool Stud 49:381–391

    Google Scholar 

  • Vergara PM, Perez-Hernandez CG, Hahn IJ, Soto GE (2013) Deforestation in central Chile causes a rapid decline in landscape connectivity for a forest specialist bird species. Ecol Res 28:481–492

    Google Scholar 

  • Vergara PM, Meneses LO, Grez AA, Quiroz MS, Soto GE, Pérez-Hernández CG, Fierro A (2017) Occupancy pattern of a long-horned beetle in a variegated forest landscape: linkages between tree quality and forest cover across spatial scales. Landsc Ecol 32:279–293

    Google Scholar 

  • Vergara PM, Soto GE, Rodewald AD, Quiroz M (2019) Behavioral switching in Magellanic woodpeckers reveals perception of habitat quality at different spatial scales. Landsc Ecol 34:79–92

    Google Scholar 

  • Vitz AC, Rodewald AD (2006) Can regenerating clearcuts benefit mature-forest songbirds? An examination of post-breeding ecology. Biol Cons 127:477–486

    Google Scholar 

  • Wagner DL (2020) Insect declines in the Anthropocene. Annu Rev Entomol 65:457–480

    CAS  PubMed  Google Scholar 

  • Waide RB, Narins PM (1988) Tropical forest bird counts and the effect of sound attenuation. Auk 105:296–302

    Google Scholar 

  • Watson DM (2011) A productivity-based explanation for woodland bird declines: poorer soils yield less food. Emu 111:10–18

    Google Scholar 

  • Watson DM (2015) Disproportionate declines in ground-foraging insectivorous birds after mistletoe removal. PLoS ONE 10(12):e0142992

    PubMed  PubMed Central  Google Scholar 

  • White JA, Whitham TG (2000) Associational susceptibility of cottonwood to a box elder herbivore. Ecology 81:175–1803

    Google Scholar 

  • Zanette L, Doyle P, Trémont SM (2000) Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 81:1654–1666

    Google Scholar 

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Acknowledgements

This study was funded by ANID-FONDECYT 1180978. We thank ANID-FONDECYT postdoctoral Grant 3180112, C. Perez-Hernández, G. Toledo, K. Norambuena and L. Meneses for their contributions in data collection and analysis. Alberto J. Alaniz and Mario A. Carvajal were supported by ANID-PFCHA/ Doctorado Nacional 2020-21201496 and 2020-21201494. Marlene Lizama thanks ANID-PFCHA/ Doctorado Nacional 2020-21201124.

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Authors and Affiliations

  1. Departamento de Gestión Agraria, Universidad de Santiago de Chile, Santiago, Chile

    Pablo M. Vergara, Andrés Fierro, Alberto J. Alaniz, Marlene Lizama & José L. Llanos

  2. Centro de Estudios en Ecología Espacial y Medio Ambiente, Ecogeografía, Santiago, Chile

    Alberto J. Alaniz & Mario A. Carvajal

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  1. Pablo M. Vergara
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  2. Andrés Fierro
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  3. Alberto J. Alaniz
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  4. Mario A. Carvajal
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  5. Marlene Lizama
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  6. José L. Llanos
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Correspondence to Pablo M. Vergara.

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Vergara, P.M., Fierro, A., Alaniz, A.J. et al. Landscape-scale effects of forest degradation on insectivorous birds and invertebrates in austral temperate forests. Landscape Ecol 36, 191–208 (2021). https://doi.org/10.1007/s10980-020-01133-2

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