in

Metabarcoding insights into the diet and trophic diversity of six declining farmland birds

  • 1.

    Tscharntke, T., Klein, A. M., Kruess, A., Steffan-Dewenter, I. & Thies, C. Landscape perspectives on agricultural intensification and biodiversity–ecosystem service management. Ecol. Lett. 8, 857–874 (2005).

    Article 

    Google Scholar 

  • 2.

    Van Zanten, B. T. et al. European agricultural landscapes, common agricultural policy and ecosystem services: A review. Agron. Sustain. Dev. 34, 309–325 (2014).

    Article 

    Google Scholar 

  • 3.

    Jongman, R. H. Homogenisation and fragmentation of the European landscape: Ecological consequences and solutions. Landsc. Urban Plan. 58, 211–221 (2002).

    Article 

    Google Scholar 

  • 4.

    Stoate, C. et al. Ecological impacts of arable intensification in Europe. J. Environ. Manag. 63, 337–365 (2001).

    CAS 
    Article 

    Google Scholar 

  • 5.

    Storkey, J., Meyer, S., Still, K. S. & Leuschner, C. The impact of agricultural intensification and land-use change on the European arable flora. Proc. R. Soc. B 279, 1421–1429 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 6.

    Donald, P. F., Sanderson, F. J., Burfield, I. J. & Van Bommel, F. P. J. Further evidence of continent-wide impacts of agricultural intensification on European farmland birds, 1990–2000. Agric. Ecosyst. Environ. 116, 189–196 (2006).

    Article 

    Google Scholar 

  • 7.

    Benton, T. G., Vickery, J. A. & Wilson, J. D. Farmland biodiversity: Is habitat heterogeneity the key?. Trends Ecol. Evol. 18, 182–188 (2003).

    Article 

    Google Scholar 

  • 8.

    Traba, J. & Morales, M. B. The decline of farmland birds in Spain is strongly associated to the loss of fallowland. Sci. Rep. 9, 1–6 (2019).

    Article 
    CAS 

    Google Scholar 

  • 9.

    Mcmahon, B. J., Giralt, D., Raurell, M., Brotons, L. & Bota, G. Identifying set-aside features for bird conservation and management in northeast Iberian pseudo-steppes. Bird Study 57, 289–300 (2010).

    Article 

    Google Scholar 

  • 10.

    Tarjuelo, R. et al. Living in seasonally dynamic farmland: The role of natural and semi-natural habitats in the movements and habitat selection of a declining bird. Biol. Conserv. 251, 108794 (2020).

    Article 

    Google Scholar 

  • 11.

    Donázar, J. A., Naveso, M. A., Tella, J. L. & Campión, D. Extensive grazing and raptors in Spain. 117–149. in Farming and Birds in Europe: The Common Agricultural Policy and Its Implications for Bird Conservation (Pain, D. J. & Pienkowski, M. W. eds.). (Academic Press, 1997).

  • 12.

    Santos, T. & Suárez, F. Biogeography and population trends of the Iberian steppe birds. in Ecology and Conservation of Steppe-Land Birds (Bota, G., Morales, M. B., Mañosa, S. & Camprodon, J. eds.). (Lynx Edicions, 2005).

  • 13.

    Tarjuelo, R., Margalida, A. & Mougeot, F. Changing the fallow paradigm: A win–win strategy for the post-2020 Common Agricultural Policy to halt farmland bird declines. J. Appl. Ecol. 57, 642–649 (2020).

    Article 

    Google Scholar 

  • 14.

    Wilson, J. D., Morris, A. J., Arroyo, B. E., Clark, S. C. & Bradbury, R. B. A review of the abundance and diversity of invertebrate and plant foods of granivorous birds in northern Europe in relation to agricultural change. Agric. Ecosyst. Environ. 75, 13–30 (1999).

    Article 

    Google Scholar 

  • 15.

    Benton, T. G., Bryant, D. M., Cole, L. & Crick, H. Q. Linking agricultural practice to insect and bird populations: A historical study over three decades. J. Appl. Ecol. 39, 673–687 (2002).

    Article 

    Google Scholar 

  • 16.

    Raven, P. H. & Wagner, D. L. Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proc. Natl. Acad. Sci. U.S.A. 118, 2 (2021).

    Article 
    CAS 

    Google Scholar 

  • 17.

    Andreasen, C., Jensen, H. A. & Jensen, S. M. Decreasing diversity in the soil seed bank after 50 years in Danish arable fields. Agric. Ecosyst. Environ. 259, 61–71 (2018).

    Article 

    Google Scholar 

  • 18.

    Newton, I. The recent declines of farmland bird populations in Britain: An appraisal of causal factors and conservation actions. Ibis 146, 579–600 (2004).

    Article 

    Google Scholar 

  • 19.

    Burfield, I. J. The conservation status of steppic birds in Europe. 119–140. in Ecology and Conservation of Steppe-Land Birds (Bota, G., Morales, M. B., Mañosa, S. & Camprodon, J. eds.). (Lynx Edicions, 2005).

  • 20.

    Del Hoyo, J., Elliott, A., Sargatal, J. & Christie D. A. Handbook of the Birds of the World. (Lynx Edicions, 1992).

  • 21.

    Madroño, A., González, C. & Atienza, J. C. Libro Rojo de las Aves de España. (Dirección General para la Biodiversidad-SEO/BirdLife, 2004)

  • 22.

    Suárez, F., Hervás, I., Levassor, C. & Casado, M. A. La alimentación de la ganga ibérica y la ganga ortega. 215–229. in La Ganga Iberica (Pterocles alchata) y la Ganga Ortega (Pterocles orientalis) en España. Distribución, Abundancia, Biología y Conservación (Herranz, J. & Suárez, F. eds.). (Ministerio de Medio Ambiente, 1999).

  • 23.

    Jiguet, F. Arthropods in diet of Little Bustards Tetrax tetrax during the breeding season in western France. Bird Study 49, 105–109 (2002).

    Article 

    Google Scholar 

  • 24.

    Bravo, C., Ponce, C., Palacín, C. & Alonso, J. C. Diet of young Great Bustards Otis tarda in Spain: Sexual and seasonal differences. Bird Study 59, 243–251 (2012).

    Article 

    Google Scholar 

  • 25.

    Pompanon, F. et al. Who is eating what: Diet assessment using next generation sequencing. Mol. Ecol. 21, 1931–1950 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 26.

    Shokralla, S., Spall, J. L., Gibson, J. F. & Hajibabaei, M. Next-generation sequencing technologies for environmental DNA research. Mol. Ecol. 21, 1794–1805 (2012).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 27.

    Mougeot, F., Fernández-Tizón, M., Tarjuelo, R., Benítez-López, A. & Jiménez, J. La Ganga Ibérica y la Ganga Ortega en España, Población Reproductora en 2019 y Método de Censo. (SEO/BirdLife, 2021).

  • 28.

    Martin, T. E. Food as a limit on breeding birds: A life-history perspective. Annu. Rev. Ecol. Evol. Syst. 18, 453–487 (1987).

    Article 

    Google Scholar 

  • 29.

    Martín, C. A., Casas, F., Mougeot, F., García, J. T. & Viñuela, J. Positive interactions between vulnerable species in agrarian pseudo-steppes: Habitat use by pin-tailed sandgrouse depends on its association with the little bustard. Anim. Conserv. 13, 383–389 (2010).

    Article 

    Google Scholar 

  • 30.

    Bravo, C., Cuscó, F., Morales, M. & Mañosa, S. Diet composition of a declining steppe bird the Little Bustard (Tetrax tetrax) in relation to farming practices. Avian Conserv. Ecol. 12, 1 (2017).

    CAS 

    Google Scholar 

  • 31.

    Morse, J. G. & Hoddle, M. S. Invasion biology of thrips. Annu. Rev. Entomol. 51, 67–89 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 32.

    Goldarazena, A. Orden Thysanoptera. Ide@-Sea 52, 1–20 (2015).

    Google Scholar 

  • 33.

    Ndang’ang’a, P. K., Njoroge, J. B. & Vickery, J. Quantifying the contribution of birds to the control of arthropod pests on kale, Brassica oleracea acephala, a key crop in East African highland farmland. Int. J. Pest Manag. 59, 211–216 (2013).

    Article 

    Google Scholar 

  • 34.

    Gunnarsson, B. Bird predation on spiders: Ecological mechanisms and evolutionary consequences. J. Arachnol. 35(509), 529 (2007).

    Google Scholar 

  • 35.

    Lee, J. H. et al. Anticancer activity of the antimicrobial peptide scolopendrasin VII derived from the centipede, Scolopendra subspinipes mutilans. J. Microbiol. Biotechnol. 25, 1275–1280 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 36.

    Lima, D. B. et al. Antiparasitic effect of Dinoponera quadriceps giant ant venom. Toxicon 120, 128–132 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 37.

    Whitman, D. W. et al. Antiparasitic properties of cantharidin and the blister beetle berberomeloe majalis (Coleoptera: meloidae). Toxins 11, 234 (2019).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • 38.

    Bravo, C., Bautista, L. M., García-París, M., Blanco, G. & Alonso, J. C. Males of a strongly polygynous species consume more poisonous food than females. PLoS ONE 9, e111057 (2014).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 39.

    Bolívar, P. et al. Antiparasitic effects of plant species from the diet of great bustards. Preprint. https://doi.org/10.21203/rs.3.rs-122399/v1 (2020).

    Article 

    Google Scholar 

  • 40.

    Boyer, A. G. et al. Seasonal variation in top-down and bottom-up processes in a grassland arthropod community. Oecologia 136, 309–316 (2003).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 41.

    Palacios, F., Garzón, J. & Castroviejo, J. L. alimentación de la avutarda (Otis tarda) en España, especialmente en primavera. Ardeola 21, 347–406 (1975).

    Google Scholar 

  • 42.

    Cabodevilla, X., Gómez-Moliner, B. J. & Madeira, M. J. Simultaneous analysis of the intestinal parasites and diet through eDNA metabarcoding. Preprint. https://doi.org/10.22541/au.158531783.33894277 (2020).

    Article 

    Google Scholar 

  • 43.

    García de la Morena, E. L., Bota, G., Mañosa, S. & Morales, M. B. El Sisón Común en España. II Censo Nacional (2016). (SEO/BirdLife, 2018).

  • 44.

    Cabodevilla, X., Aebischer, N. J., Mougeot, F., Morales, M. B. & Arroyo, B. Are population changes of endangered little bustards associated with releases of red-legged partridges for hunting? A large-scale study from central Spain. Eur. J. Wildl. Res. 66, 1–10 (2020).

    Article 

    Google Scholar 

  • 45.

    Cuscó, F., Cardador, L., Bota, G., Morales, M. B. & Mañosa, S. Inter-individual consistency in habitat selection patterns and spatial range constraints of female little bustards during the non-breeding season. BMC Ecol. 18, 1–12 (2018).

    Article 

    Google Scholar 

  • 46.

    González del Portillo, D., Arroyo, B., García Simón, G. & Morales, M. B. Can current farmland landscapes feed declining steppe birds? Evaluating arthropod abundance for the endangered little bustard (Tetrax tetrax) in cereal farmland during the chick‐rearing period: Variations between habitats and localities. Ecol. Evol. 11, 3219–3238 (2021).

  • 47.

    Silva, J. P., Pinto, M. & Palmeirim, J. M. Managing landscapes for the little bustard Tetrax tetrax: Lessons from the study of winter habitat selection. Biol. Conserv. 117, 521–528 (2004).

    Article 

    Google Scholar 

  • 48.

    Pfiffner, L. & Luka, H. Overwintering of arthropods in soils of arable fields and adjacent semi-natural habitats. Agric. Ecosyst. Environ. 78, 215–222 (2000).

    Article 

    Google Scholar 

  • 49.

    Hendrickx, F. et al. How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J. Appl. Ecol. 44, 340–351 (2007).

    Article 

    Google Scholar 

  • 50.

    Tarjuelo, R., Morales, M. B., Arribas, L. & Traba, J. Abundance of weeds and seeds but not of arthropods differs between arable habitats in an extensive Mediterranean farming system. Ecol. Res. 34, 624–636 (2019).

    Article 

    Google Scholar 

  • 51.

    Green, R. E. The feeding ecology and survival of partridge chicks (Alectoris rufa and Perdix perdix) on arable farmland in East Anglia. J. Appl. Ecol. 1, 817–830 (1984).

    Article 

    Google Scholar 

  • 52.

    Palacín, C. La decadencia de la comunidad de aves de los cultivos cerealistas mediterráneos. in XV Congreso del Grupo Ibérico de Aguiluchos. https://xvcongresoaguiluchosgia.es/wp-content/uploads/2019/11/LA-DECADENCIA-DE-LA-COMUNIDAD-DE-AVES-DE-LOS-CULTIVOS-CEREALISTAS-MEDITERRÁNEOS-Carlos-Palac%C3%ADn.pdf (2019).

  • 53.

    Blanco-Aguiar, J. A., Virgós, E. & Villafuerte, R. Perdiz roja (Alectoris rufa). in Atlas de las Aves Reproductoras de España. 212–213 (2003).

  • 54.

    Rodríguez-Teijeiro, J. D., Puigcerver, M. & Gallego, S. Codorniz común. in Atlas de las Aves Reproductoras de España. 218–219 (2003).

  • 55.

    Andueza, A. et al. Evaluación del Impacto Económico y Social de la Caza en España. (Fundación Artemisan, 2018)

  • 56.

    Lane, S. J., Alonso, J. C., Alonso, J. A. & Naveso, M. A. Seasonal changes in diet and diet selection of great bustards (Otis tarda) in north-west Spain. J. Zool. 247, 201–214 (1999).

    Article 

    Google Scholar 

  • 57.

    QGIS Development Team. QGIS Geographic Information System. http://qgis.osgeo.org (Open Source Geospatial Foundation Project, 2018).

  • 58.

    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).

    Article 

    Google Scholar 

  • 59.

    Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    CAS 
    Article 

    Google Scholar 

  • 60.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic. Acids Res. 41, D590–D596 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 61.

    McKnight, D. T. et al. Methods for normalizing microbiome data: An ecological perspective. Methods Ecol. Evol. 10, 389–400 (2019).

    Article 

    Google Scholar 

  • 62.

    Lamb, P. D. et al. How quantitative is metabarcoding: A meta-analytical approach. Mol. Ecol. 28, 420–430 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Piñol, J., Senar, M. A. & Symondson, W. O. The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative. Mol. Ecol. 28, 407–419 (2019).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 64.

    Russo, T. et al. All is fish that comes to the net: metabarcoding for rapid fisheries catch assessment. Ecol. Appl. 31, e02273 (2021).

    ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 65.

    González-Teuber, M., Vilo, C., Guevara-Araya, M. J., Salgado-Luarte, C. & Gianoli, E. Leaf resistance traits influence endophytic fungi colonization and community composition in a South American temperate rainforest. J. Ecol. 108, 1019–1029 (2020).

    Article 
    CAS 

    Google Scholar 

  • 66.

    Aliche, E. B., Talsma, W., Munnik, T. & Bouwmeester, H. J. Characterization of maize root microbiome in two different soils by minimizing plant DNA contamination in metabarcoding analysis. Biol. Fertil. Soils. 57, 731–737 (2021).

    CAS 
    Article 

    Google Scholar 

  • 67.

    de Groot, G. A. et al. The aerobiome uncovered: Multi-marker metabarcoding reveals potential drivers of turn-over in the full microbial community in the air. Environ. Int. 154, 106551 (2021).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 68.

    Tordoni, E. et al. Integrated eDNA metabarcoding and morphological analyses assess spatio-temporal patterns of airborne fungal spores. Ecol. Indic. 121, 107032 (2021).

    Article 

    Google Scholar 

  • 69.

    R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/. (R Foundation for Statistical Computing, 2019).

  • 70.

    Russell, V. L. Least-squares means: The R Package lsmeans. J. Stat. Softw. 69, 1–33 (2016).

    Google Scholar 

  • 71.

    Oksanen, J. et al. Vegan: Community Ecology Package. R Package Version 2.0 (2013).


  • Source: Ecology - nature.com

    Eat me, or don’t eat me?

    MIT Energy Initiative awards seven Seed Fund grants for early-stage energy research