Food web transfer of plastics to an apex riverine predator.
birds
food webs
microplastics
pollution
river ecosystems
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
24
11
2019
revised:
27
03
2020
accepted:
18
04
2020
pubmed:
23
5
2020
medline:
27
11
2020
entrez:
23
5
2020
Statut:
ppublish
Résumé
As a rapidly accelerating expression of global change, plastics now occur extensively in freshwater ecosystems, yet there is barely any evidence of their transfer through food webs. Following previous observations that plastics occur widely in their prey, we used a field study of free-living Eurasian dippers (Cinclus cinclus), to test the hypotheses that (1) plastics are transferred from prey to predators in rivers, (2) plastics contained in prey are transferred by adults to altricial offspring during provisioning and (3) plastic concentrations in faecal and regurgitated pellets from dippers increase with urbanization. Plastic occurred in 50% of regurgitates (n = 74) and 45% of faecal samples (n = 92) collected non-invasively from adult and nestling dippers at 15 sites across South Wales (UK). Over 95% of particles were fibres, and concentrations in samples increased with urban land cover. Fourier transform infrared spectroscopy identified multiple polymers, including polyester, polypropylene, polyvinyl chloride and vinyl chloride copolymers. Although characterized by uncertainty, steady-state models using energetic data along with plastic concentration in prey and excreta suggest that around 200 plastic particles are ingested daily by dippers, but also excreted at rates that suggest transitory throughput. As some of the first evidence revealing that plastic is now being transferred through freshwater food webs, and between adult passerines and their offspring, these data emphasize the need to appraise the potential ecotoxicological consequences of increasing plastic pollution.
Substances chimiques
Plastics
0
Water Pollutants, Chemical
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3846-3857Informations de copyright
© 2020 The Authors. Global Change Biology published by John Wiley & Sons Ltd.
Références
Allen, S., Allen, D., Phoenix, V. R., Le Roux, G., Jiménez, P. D., Simonneau, A., … Galop, D. (2019). Atmospheric transport and deposition of microplastics in a remote mountain catchment. Nature Geoscience, 12, 339-344. https://doi.org/10.1038/s41561-019-0335-5
Amélineau, F., Bonnet, D., Heitz, O., Mortreux, V., Harding, A. M. A., Karnovsky, N., … Grémillet, D. (2016). Microplastic pollution in the Greenland Sea: Background levels and selective contamination of planktivorous diving seabirds. Environmental Pollution, 219, 1131-1139. https://doi.org/10.1016/j.envpol.2016.09.017
Andrade, M. C., Winemiller, K. O., Barbosa, P. S., Fortunati, A., Chelazzi, D., Cincinelli, A., & Giarrizzo, T. (2019). First account of plastic pollution impacting freshwater fishes in the Amazon: Ingestion of plastic debris by piranhas and other serrasalmids with diverse feeding habits. Environmental Pollution, 244, 766-773. https://doi.org/10.1016/j.envpol.2018.10.088
Au, S. Y., Bruce, T. F., Bridges, W. C., & Klaine, S. J. (2015). Responses of Hyalella azteca to acute and chronic microplastic exposure. Environmental Toxicology and Chemistry, 34, 2564-2572. https://doi.org/10.1002/etc.3093
Barnes, D. K., Galgani, F., Thompson, R. C., & Barlaz, M. (2009). Accumulation and fragmentation of plastic debris in global environments. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 1985-1998. https://doi.org/10.1098/rstb.2008.0205
Biginagwa, F. J., Mayoma, B. S., Shashoua, Y., Syberg, K., & Khan, F. R. (2016). First evidence of microplastics in the African Great Lakes: Recovery from Lake Victoria Nile perch and Nile tilapia. Journal of Great Lakes Research, 42, 146-149. https://doi.org/10.1016/j.jglr.2015.10.012
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., & White, J.-S.-S. (2009). Generalized linear mixed models: A practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127-135. https://doi.org/10.1016/j.tree.2008.10.008
Bryant, D. M., & Bryant, V. M. T. (1988). Assimilation efficiency and growth of nestling insectivores. Ibis, 130, 268-274. https://doi.org/10.1111/j.1474-919X.1988.tb00977.x
Bryant, D. M., & Hails, C. J. (1983). Energetics and growth patterns of three tropical bird species. The Auk, 100, 425-439. https://doi.org/10.1093/auk/100.2.425
Bryant, D. M., & Tatner, P. (1988). Energetics of the annual cycle of dippers Cinclus cinclus. Ibis, 130, 17-38. https://doi.org/10.1111/j.1474-919X.1988.tb00952.x
Brydson, J. A. (1999). Vinyl chloride polymers. In J. A. Brydson (Ed.), Plastics materials (pp. 311-362). Amsterdam, the Netherlands: Elsevier. https://doi.org/10.1016/B978-0-408-00721-4.50016-3
Buckton, S. T., & Ormerod, S. J. (2008). Niche segregation of Himalayan river birds. Journal of Field Ornithology, 79, 176-185. https://doi.org/10.1111/j.1557-9263.2008.00160.x
Cai, L., Wang, J., Peng, J., Tan, Z., Zhan, Z., Tan, X., & Chen, Q. (2017). Characteristic of microplastics in the atmospheric fallout from Dongguan city, China: Preliminary research and first evidence. Environmental Science and Pollution Research, 24, 24928-24935. https://doi.org/10.1007/s11356-019-06979-x
Carey, M. J. (2011). Intergenerational transfer of plastic debris by Short-tailed Shearwaters (Ardenna tenuirostris). Emu - Austral Ornithology, 111, 229-234. https://doi.org/10.1071/MU10085
Claessens, M., De Meester, S., Van Landuyt, L., De Clerck, K., & Janssen, C. R. (2011). Occurrence and distribution of microplastics in marine sediments along the Belgian coast. Marine Pollution Bulletin, 62, 2199-2204. https://doi.org/10.1016/j.marpolbul.2011.06.030
Corcoran, P. L., Norris, T., Ceccanese, T., Walzak, M. J., Helm, P. A., & Marvin, C. H. (2015). Hidden plastics of Lake Ontario, Canada and their potential preservation in the sediment record. Environmental Pollution, 204, 17-25. https://doi.org/10.1016/j.envpol.2015.04.009
de Souza Machado, A. A., Kloas, W., Zarfl, C., Hempel, S., & Rillig, M. C. (2018). Microplastics as an emerging threat to terrestrial ecosystems. Global Change Biology, 24, 1405-1416. https://doi.org/10.1111/gcb.14020
Dris, R., Gasperi, J., Saad, M., Mirande, C., & Tassin, B. (2016). Synthetic fibers in atmospheric fallout: A source of microplastics in the environment? Marine Pollution Bulletin, 104, 290-293. https://doi.org/10.1016/j.marpolbul.2016.01.006
Duis, K., & Coors, A. (2016). Microplastics in the aquatic and terrestrial environment: Sources (with a specific focus on personal care products), fate and effects. Environmental Sciences Europe, 28, 2. https://doi.org/10.1186/s12302-015-0069-y
Farrell, P., & Nelson, K. (2013). Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Environmental Pollution, 177, 1-3. https://doi.org/10.1016/j.envpol.2013.01.046
Foekema, E. M., De Gruijter, C., Mergia, M. T., van Franeker, J. A., Murk, A. J., & Koelmans, A. A. (2013). Plastic in North Sea fish. Environmental Science & Technology, 47, 8818-8824. https://doi.org/10.1021/es400931b
Foley, C. J., Feiner, Z. S., Malinich, T. D., & Höök, T. O. (2018). A meta-analysis of the effects of exposure to microplastics on fish and aquatic invertebrates. Science of the Total Environment, 631-632, 550-559. https://doi.org/10.1016/j.scitotenv.2018.03.046
Geyer, R., Jambeck, J. R., & Law, K. L. (2017). Production, use, and fate of all plastics ever made. Science Advances, 3, e1700782. https://doi.org/10.1126/sciadv.1700782
Gil-Delgado, J. A., Guijarro, D., Gosálvez, R. U., López-Iborra, G. M., Ponz, A., & Velasco, A. (2017). Presence of plastic particles in waterbirds faeces collected in Spanish lakes. Environmental Pollution, 220, 732-736. https://doi.org/10.1016/j.envpol.2016.09.054
Holland, E. R., Mallory, M. L., & Shutler, D. (2016). Plastics and other anthropogenic debris in freshwater birds from Canada. Science of the Total Environment, 571, 251-258. https://doi.org/10.1016/j.scitotenv.2016.07.158
Horton, A. A., Jürgens, M. D., Lahive, E., van Bodegom, P. M., & Vijver, M. G. (2018). The influence of exposure and physiology on microplastic ingestion by the freshwater fish Rutilus rutilus (roach) in the River Thames, UK. Environmental Pollution, 236, 7. https://doi.org/10.1016/j.envpol.2018.01.044
Horton, A. A., Svendsen, C., Williams, R. J., Spurgeon, D. J., & Lahive, E. (2017). Large microplastic particles in sediments of tributaries of the River Thames, UK - Abundance, sources and methods for effective quantification. Marine Pollution Bulletin, 114, 218-226. https://doi.org/10.1016/j.marpolbul.2016.09.004
Horton, A. A., Walton, A., Spurgeon, D. J., Lahive, E., & Svendsen, C. (2017). Microplastics in freshwater and terrestrial environments: Evaluating the current understanding to identify the knowledge gaps and future research priorities. Science of the Total Environment, 586, 127-141. https://doi.org/10.1016/j.scitotenv.2017.01.190
Hurley, R. R., Woodward, J. C., & Rothwell, J. J. (2017). Ingestion of microplastics by freshwater Tubifex tubifex worms. Environmental Science & Technology, 51, 12844-12851. https://doi.org/10.1021/acs.est.7b03567
Hurley, R., Woodward, J., & Rothwell, J. J. (2018). Microplastic contamination of river beds significantly reduced by catchment-wide flooding. Nature Geoscience, 11(4), 251-257. https://doi.org/10.1038/s41561-018-0080-1
Imhof, H. K., Ivleva, N. P., Schmid, J., Niessner, R., & Laforsch, C. (2013). Contamination of beach sediments of a subalpine lake with microplastic particles. Current Biology, 23, 867-868. https://doi.org/10.1016/j.cub.2013.09.001
Jambeck, J. R., Geyer, R., Wilcox, C., Siegler, T. R., Perryman, M., Andrady, A., … Law, K. L. (2015). Plastic waste inputs from land into the ocean. Science, 347, 768-771. https://doi.org/10.1126/science.1260352
Jeong, C. B., Won, E. J., Kang, H. M., Lee, M. C., Hwang, D. S., Hwang, U. K., … Lee, J.-S. (2016). Microplastic size-dependent toxicity, oxidative stress induction, and p-JNK and p-p38 activation in the monogonont rotifer (Brachionus koreanus). Environmental Science & Technology, 50, 8849-8857. https://doi.org/10.1021/acs.est.6b01441
JNCC (2010). Handbook of phase 1 habitat survey - a technique for environmental audit. Peterborough, UK: JNCC.
Kelly, B. C., Ikonomou, M. G., Blair, J. D., Morin, A. E., & Gobas, F. A. P. C. (2007). Food web-specific biomagnification of persistent organic pollutants. Science, 317, 236-239. https://doi.org/10.1126/science.1138275
Lechner, A., Keckeis, H., Lumesberger-Loisl, F., Zens, B., Krusch, R., Tritthart, M., … Schludermann, E. (2014). The Danube so colourful: A potpourri of plastic litter outnumbers fish larvae in Europe's second largest river. Environmental Pollution, 188, 177-181. https://doi.org/10.1016/j.envpol.2014.02.006
Lehner, B., & Grill, G. (2013). Global river hydrography and network routing: Baseline data and new approaches to study the world’s large river systems. Hydrological Processes, 27, 2171-2186. https://doi.org/10.1002/hyp.9740
Löder, M. G. J., & Gerdts, G. (2015). Methodology used for the detection and identification of microplastics - A critical appraisal. In M. Bergmann, L. Gutlow, & M. Klages (Eds.), Marine anthropogenic litter (pp. 201-227). Cham: Springer. https://doi.org/10.1007/978-3-319-16510-3_8
Maes, T., Jessop, R., Wellner, N., Haupt, K., & Mayes, A. G. (2017). A rapid-screening approach to detect and quantify microplastics based on fluorescent tagging with Nile Red. Scientific Reports, 7, 44501. https://doi.org/10.1038/srep44501
McKeen, L. W. (2012). Polyvinyls and acrylics. In L. W. McKeen (Ed.), Film properties of plastics and elastomers (pp. 219-254). Amsterdam, the Netherlands: Elsevier. https://doi.org/10.1016/B978-1-4557-2551-9.00010-4
McNeish, R. E., Kim, L. H., Barrett, H. A., Mason, S. A., Kelly, J. J., & Hoellein, T. J. (2018). Microplastic in riverine fish is connected to species traits. Scientific Reports, 8, 11639. https://doi.org/10.1038/s41598-018-29980-9
Moore, C. J., Lattin, G. L., & Zellers, A. F. (2011). Quantity and type of plastic debris flowing from two urban rivers to coastal waters and beaches of Southern California. Journal of Integrated Coastal Zone Management, 11, 65-73. https://doi.org/10.5894/rgci194
Morrissey, C. A., Boldt, A., Mapstone, A., Newton, J., & Ormerod, S. J. (2013). Stable isotopes as indicators of wastewater effects on the macroinvertebrates of urban rivers. Hydrobiologia, 700, 231-244. https://doi.org/10.1007/s10750-012-1233-7
Morrissey, C. A., Elliott, J. E., & Ormerod, S. J. (2010). Local to continental influences on nutrient and contaminant sources to river birds. Environmental Science & Technology, 44, 1860-1867. https://doi.org/10.1021/es903084m
Morrissey, C. A., Stanton, D. W. G., Pereira, M. G., Newton, J., Durance, I., Tyler, C. R., & Ormerod, S. J. (2013). Eurasian dipper eggs indicate elevated organohalogenated contaminants in urban rivers. Environmental Science & Technology, 47, 8931-8939. https://doi.org/10.1021/es402124z
Morrissey, C. A., Stanton, D. W. G., Tyler, C. R., Pereira, M. G., Newton, J., Durance, I., & Ormerod, S. J. (2014). Developmental impairment in Eurasian dipper nestlings exposed to urban stream pollutants. Environmental Toxicology and Chemistry, 33, 1315-1323. https://doi.org/10.1002/etc.2555
Nelms, S. E., Galloway, T. S., Godley, B. J., Jarvis, D. S., & Lindeque, P. K. (2018). Investigating microplastic trophic transfer in marine top predators. Environmental Pollution, 238, 999-1007. https://doi.org/10.1016/j.envpol.2018.02.016
Ng, K. L., & Obbard, J. P. (2006). Prevalence of microplastics in Singapore’s coastal marine environment. Marine Pollution Bulletin, 52, 761-767. https://doi.org/10.1016/j.marpolbul.2005.11.017
Nobre, C. R., Santana, M. F. M., Maluf, A., Cortez, F. S., Cesar, A., Pereira, C. D. S., & Turra, A. (2015). Assessment of microplastic toxicity to embryonic development of the sea urchin Lytechinus variegatus (Echinodermata: Echinoidea). Marine Pollution Bulletin, 92, 99-104. https://doi.org/10.1016/j.marpolbul.2014.12.050
Ormerod, S. J. (1985). The diet of breeding dippers Cinclus cinclus and their nestlings in the catchment of the River Wye, mid-Wales: A preliminary study by faecal analysis. Ibis, 127, 316-331. https://doi.org/10.1111/j.1474-919X.1985.tb05073.x
Ormerod, S. J., Efteland, S., & Gabrielsen, L. E. (1987). The diet of breeding dippers Cinclus cinclus and their nestlings in southwestern Norway. Ecography, 10, 201-205. https://doi.org/10.1111/j.1600-0587.1987.tb00760.x
Ormerod, S. J., & Tyler, S. J. (1991). Exploitation of prey by a river bird, the dipper Cinclus cinclus (L.), along acidic and circumneutral streams in upland Wales. Freshwater Biology, 25, 105-116. https://doi.org/10.1111/j.1365-2427.1991.tb00477.x
Peters, C. A., & Bratton, S. P. (2016). Urbanization is a major influence on microplastic ingestion by sunfish in the Brazos River Basin, Central Texas, USA. Environmental Pollution, 210, 380-387. https://doi.org/10.1016/j.envpol.2016.01.018
Primpke, S., Lorenz, C., Rascher-Friesenhausen, R. R., & Gerdts, G. (2017). An automated approach for microplastics analysis using focal plane array (FPA) FTIR microscopy and image analysis. Analytical Methods, 9, 1499-1511. https://doi.org/10.1039/C6AY02476A
Provencher, J. F., Ammendolia, J., Rochman, C. M., & Mallory, M. L. (2019). Assessing plastic debris in aquatic food webs: What we know and don’t know about uptake and trophic transfer. Environmental Reviews, 27, 304-317. https://doi.org/10.1139/er-2018-0079
R Core Team. (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Redondo-Hasselerharm, P. E., Falahudin, D., Peeters, E. T. H. M., & Koelmans, A. A. (2018). Microplastic effect thresholds for freshwater benthic macroinvertebrates. Environmental Science & Technology, 52, 2278-2286. https://doi.org/10.1021/acs.est.7b05367
Rehse, S., Kloas, W., & Zarfl, C. (2016). Short-term exposure with high concentrations of pristine microplastic particles leads to immobilisation of Daphnia magna. Chemosphere, 153, 91-99. https://doi.org/10.1016/j.chemosphere.2016.02.133
Reynolds, C., & Ryan, P. G. (2018). Micro-plastic ingestion by waterbirds from contaminated wetlands in South Africa. Marine Pollution Bulletin, 126, 330-333. https://doi.org/10.1016/j.marpolbul.2017.11.021
Rillig, M. C. (2012). Microplastic in terrestrial ecosystems and the soil? Environmental Science & Technology, 46, 6453-6454. https://doi.org/10.1021/es302011r
Rochman, C. M., Browne, M. A., Halpern, B. S., Hentschel, B. T., Hoh, E., Karapanagioti, H. K., … Thompson, R. C. (2013). Classify plastic waste as hazardous. Nature, 494, 169-171. https://doi.org/10.1038/494169a
Rosenkranz, P., Chaudhry, Q., Stone, V., & Fernandes, T. F. (2009). A comparison of nanoparticle and fine particle uptake by Daphnia magna. Environmental Toxicology and Chemistry, 28, 2142-2149. https://doi.org/10.1897/08-559.1
Ruxton, G. D., & Beauchamp, G. (2008). Some suggestions about appropriate use of the Kruskal-Wallis test. Animal Behaviour, 76, 1083-1087. https://doi.org/10.1016/j.anbehav.2008.04.011
Sanchez, W., Bender, C., & Porcher, J. M. (2014). Wild gudgeons (Gobio gobio) from French rivers are contaminated by microplastics: Preliminary study and first evidence. Environmental Research, 128, 98-100. https://doi.org/10.1016/j.envres.2013.11.004
Setälä, O., Fleming-Lehtinen, V., & Lehtiniemi, M. (2014). Ingestion and transfer of microplastics in the planktonic food web. Environmental Pollution, 185, 77-83. https://doi.org/10.1016/j.envpol.2013.10.013
Silva-Cavalcanti, J. S., Silva, J. D. B., de França, E. J., de Araújo, M. C. B., & Gusmão, F. (2017). Microplastics ingestion by a common tropical freshwater fishing resource. Environmental Pollution, 221, 218-226. https://doi.org/10.1016/j.envpol.2016.11.068
Stanton, T., Johnson, M., Nathanail, P., MacNaughtan, W., & Gomes, R. L. (2019). Freshwater and airborne textile fibre populations are dominated by ‘natural’, not microplastic, fibres. Science of the Total Environment, 666, 377-389. https://doi.org/10.1016/j.scitotenv.2019.02.278
Sussarellu, R., Suquet, M., Thomas, Y., Lambert, C., Fabioux, C., Pernet, M. E. J., … Huvet, A. (2016). Oyster reproduction is affected by exposure to polystyrene microplastics. Proceedings of the National Academy of Sciences of the United States of America, 113, 2430-2435. https://doi.org/10.1073/pnas.1519019113
Thompson, R. C., Olsen, Y., Mitchell, R. P., Davis, A., Rowland, S. J., John, A. W. G., … Russell, A. E. (2004). Lost at sea: Where is all the plastic? Science, 304, 838. https://doi.org/10.1126/science.1094559
Tyler, S. J., & Ormerod, S. J. (1994). The dippers. London, UK: Poyser. https://doi.org/10.5040/9781472597274
Vaughan, I. P., & Ormerod, S. J. (2012). Large-scale, long-term trends in British river macroinvertebrates. Global Change Biology, 18, 2184-2194. https://doi.org/10.1111/j.1365-2486.2012.02662.x
Vianello, A., Boldrin, A., Guerriero, P., Moschino, V., Rella, R., Sturaro, A., & Da Ros, L. (2013). Microplastic particles in sediments of Lagoon of Venice, Italy: First observations on occurrence, spatial patterns and identification. Estuarine, Coastal and Shelf Science, 130, 54-61. https://doi.org/10.1016/j.ecss.2013.03.022
Wagner, M., Scherer, C., Alvarez-Muñoz, D., Brennholt, N., Bourrain, X., Buchinger, S., … Reifferscheid, G. (2014). Microplastics in freshwater ecosystems: What we know and what we need to know. Environmental Sciences Europe, 26, 12. https://doi.org/10.1186/s12302-014-0012-7
Wang, J., Peng, J., Tan, Z., Gao, Y., Zhan, Z., Chen, Q., & Cai, L. (2017). Microplastics in the surface sediments from the Beijiang River littoral zone: Composition, abundance, surface textures and interaction with heavy metals. Chemosphere, 171, 248-258. https://doi.org/10.1016/j.chemosphere.2016.12.074
Watts, A. J., Urbina, M. A., Corr, S., Lewis, C., & Galloway, T. S. (2015). Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environmental Science & Technology, 49, 14597-14604. https://doi.org/10.1021/acs.est.5b04026
Windsor, F. M., Durance, I., Horton, A. A., Thompson, R. C., Tyler, C. R., & Ormerod, S. J. (2019). A catchment perspective of plastic pollution. Global Change Biology, 25, 1207-1221. https://doi.org/10.1111/gcb.14572
Windsor, F. M., Ormerod, S. J., & Tyler, C. R. (2018). Endocrine disruption in aquatic systems: Up-scaling research to address ecological consequences. Biological Reviews, 93, 626-641. https://doi.org/10.1111/brv.12360
Windsor, F. M., Pereira, M. G., Tyler, C. R., & Ormerod, S. J. (2019). Persistent contaminants as potential constraints on the recovery of urban river food webs from gross pollution. Water Research, 163, 114858. https://doi.org/10.1016/j.watres.2019.114858
Windsor, F. M., Tilley, R. M., Tyler, C. R., & Ormerod, S. J. (2019). Microplastic ingestion by riverine macroinvertebrates. Science of the Total Environment, 646, 68-74. https://doi.org/10.1016/j.scitotenv.2018.07.271
Yin, S., Tuladhar, R., Shi, F., Combe, M., Collister, T., & Sivakugan, N. (2015). Use of macro plastic fibres in concrete: A review. Construction and Building Materials, 93, 180-188. https://doi.org/10.1016/j.conbuildmat.2015.05.105
Zhao, S., Zhu, L., & Li, D. (2016). Microscopic anthropogenic litter in terrestrial birds from Shanghai, China: Not only plastics but also natural fibres. Science of the Total Environment, 550, 1110-1115. https://doi.org/10.1016/j.scitotenv.2016.01.112
Zuur, A. F., Leno, E. N., & Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1, 3-14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Zuur, A. F., Leno, E. N., & Smith, G. M. (2007). Analysing ecological data. New York: Springer, 672 pp. https://doi.org/10.1007/978-0-387-45972-1
Zuur, A. F., Leno, E. N., Walker, N. J., Saveliev, A. A., & Smith, G. M. (2009). Zero-truncated and zero-inflated models for count data. In A. F. Zuur, E. N. Leno, N. J. Walker, A. A. Saveliev, & G. M. Smith (Eds.), Mixed effects models and extensions in ecology with R (pp. 261-293). New York: Springer. https://doi.org/10.1007/978-0-387-87458-6_11