The resilience of weed seedbank regulation by carabid beetles, at continental scales, to alternative prey

. 2020 Nov 09 ; 10 (1) : 19315. [epub] 20201109

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33168869

Grantová podpora
P 28578 Austrian Science Fund FWF - Austria

Odkazy

PubMed 33168869
PubMed Central PMC7652833
DOI 10.1038/s41598-020-76305-w
PII: 10.1038/s41598-020-76305-w
Knihovny.cz E-zdroje

Carabids are generalist predators that contribute to the agricultural ecosystem service of seedbank regulation via weed seed predation. To facilitate adoption of this ecosystem services by farmers, knowledge of weed seed predation and the resilience of seedbank regulation with co-varying availability of alternative prey is crucial. Using assessments of the seedbank and predation on seed cards in 57 cereal fields across Europe, we demonstrate a regulatory effect on the soil seedbank, at a continental scale, by groups formed of omnivore, seed-eating (granivore + omnivore) and all species of carabids just prior to the crop-harvest. Regulation was associated with a positive relationship between the activity-density of carabids and seed predation, as measured on seed cards. We found that per capita seed consumption on the cards co-varied negatively with the biomass of alternative prey, i.e. Aphididae, Collembola and total alternative prey biomass. Our results underline the importance of weed seedbank regulation by carabids, across geographically significant scales, and indicate that the effectiveness of this biocontrol may depend on the availability of alternative prey that disrupt the weed seed predation.

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Begg GS, et al. A functional overview of conservation biological control. Crop Prot. 2017;97:145–158. doi: 10.1016/j.cropro.2016.11.008. DOI

Shields MW, et al. History, current situation and challenges for conservation biological control. Biol. Control. 2019;131:25–35. doi: 10.1016/j.biocontrol.2018.12.010. DOI

Petit S, Boursault A, Bohan DA. Weed seed choice by carabid beetles (Coleoptera: Carabidae): Linking field measurements with laboratory diet assessments. Eur. J. Entomol. 2014;111:1–6. doi: 10.14411/eje.2014.086. DOI

Saska P, Honěk A, Martinková Z. Preferences of carabid beetles (Coleoptera: Carabidae) for herbaceous seeds. Acta Zool. Acad. Sci. Hung. 2019;65:57–76. doi: 10.17109/AZH.65.Suppl.57.2019. DOI

Honěk A, Martinkova Z, Saska P, Pekar S. Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera) Basic Appl. Ecol. 2007;8:343–353. doi: 10.1016/j.baae.2006.07.002. DOI

Honěk A, Martinkova Z, Jarosik V. Ground beetles (Carabidae) as seed predators. Eur. J. Entomol. 2003;100:531–544. doi: 10.14411/eje.2003.081. DOI

Kulkarni SS, Dosdall LM, Willenborg CJ. The role of ground beetles (Coleoptera: Carabidae) in weed seed consumption: A review. Weed Sci. 2015;63:355–376. doi: 10.1614/WS-D-14-00067.1. DOI

Petit S, Trichard A, Biju-Duval L, McLaughlin B, Bohan DA. Interactions between conservation agricultural practice and landscape composition promote weed seed predation by invertebrates. Agric. Ecosyst. Environ. 2017;240:45–53. doi: 10.1016/j.agee.2017.02.014. DOI

Kromp B. Carabid beetles in sustainable agriculture: A review on pest control efficacy, cultivation impacts and enhancement. Agric. Ecosyst. Environ. 1999;74:187–228. doi: 10.1016/S0167-8809(99)00037-7. DOI

Firbank LG, Watkinson AR. On the analysis of competition within two-species mixtures of plants. J. Appl. Ecol. 1985;22:503–517. doi: 10.2307/2403181. DOI

Westerman PR, et al. Are many little hammers effective? Velvetleaf (Abutilon theophrasti) population dynamics in two- and four-year crop rotation systems. Weed Sci. 2005;53:382–392. doi: 10.1614/WS-04-130R. DOI

Petit S, et al. Biodiversity-based options for arable weed management. A review. Agron. Sustain. Dev. 2018;38:48. doi: 10.1007/s13593-018-0525-3. DOI

Westerman PR, Dixon PM, Liebman M. Burial rates of surrogate seeds in arable fields. Weed Res. 2009;49:142–152. doi: 10.1111/j.1365-3180.2008.00684.x. DOI

Trichard A, Ricci B, Ducourtieux C, Petit S. The spatio-temporal distribution of weed seed predation differs between conservation agriculture and conventional tillage. Agric. Ecosyst. Environ. 2014;188:40–47. doi: 10.1016/j.agee.2014.01.031. DOI

Carbonne B, Bohan DA, Petit S. Key carabid species drive spring weed seed predation of Viola arvensis. Biol. Control. 2020;141:104148. doi: 10.1016/j.biocontrol.2019.104148. DOI

Westerman PR, Wes JS, Kropff MJ, Van Der Werf W. Annual losses of weed seeds due to predation in organic cereal fields. J. Appl. Ecol. 2003;40:824–836. doi: 10.1046/j.1365-2664.2003.00850.x. DOI

Blubaugh CK, Kaplan I. Invertebrate seed predators reduce weed emergence following seed rain. Weed Sci. 2016;64:80–86. doi: 10.1614/WS-D-15-00111.1. DOI

Pannwitt H, Westerman PR, Gerowitt B. Post-dispersal seed predation can limit the number of seedlings of Echinochloa crus-galli. Biol. Control. 2019;143:95–98.

Bohan DA, Boursault A, Brooks DR, Petit S. National-scale regulation of the weed seedbank by carabid predators. J. Appl. Ecol. 2011;48:888–898. doi: 10.1111/j.1365-2664.2011.02008.x. DOI

Saska P, Van Der Werf W, De Vries E, Westerman PR. Spatial and temporal patterns of carabid activity-density in cereals do not explain levels of predation on weed seeds. Bull. Entomol. Res. 2008;98:169–181. doi: 10.1017/S0007485307005512. PubMed DOI

Mauchline AL, Watson SJ, Brown VK, Froud-Williams RJ. Post-dispersal seed predation of non-target weeds in arable crops. Weed Res. 2005;45:157–164. doi: 10.1111/j.1365-3180.2004.00443.x. DOI

Davis AS, Raghu S. Weighing abiotic and biotic influences on weed seed predation. Weed Res. 2010;50:402–412. doi: 10.1111/j.1365-3180.2010.00790.x. DOI

Davis AS, Taylor EC, Haramoto ER, Renner KA. Annual postdispersal weed seed predation in contrasting field environments. Weed Sci. 2013;61:296–302. doi: 10.1614/WS-D-12-00157.1. DOI

Lövei GL, Szentkiralyi F. Carabids climbing maize plants. Z. Angew. Entomol. 1984;97:107–110. doi: 10.1111/j.1439-0418.1984.tb03722.x. DOI

Frei B, Guenay Y, Bohan DA, Traugott M, Wallinger C. Molecular analysis indicates high levels of carabid weed seed consumption in cereal fields across Central Europe. J. Pest Sci. 2019;2004(92):935–942. doi: 10.1007/s10340-019-01109-5. PubMed DOI PMC

Roubinet E, et al. High redundancy as well as complementary prey choice characterize generalist predator food webs in agroecosystems. Sci. Rep. 2018;8:8054. doi: 10.1038/s41598-018-26191-0. PubMed DOI PMC

Staudacher K, et al. Habitat heterogeneity induces rapid changes in the feeding behaviour of generalist arthropod predators. Funct. Ecol. 2018;32:809–819. doi: 10.1111/1365-2435.13028. PubMed DOI PMC

Evans EW. Multitrophic interactions among plants, aphids, alternate prey and shared natural enemies - A review. Eur. J. Entomol. 2008;105:369–380. doi: 10.14411/eje.2008.047. DOI

Snyder WE. Give predators a complement: Conserving natural enemy biodiversity to improve biocontrol. Biol. Control. 2019;135:73–82. doi: 10.1016/j.biocontrol.2019.04.017. DOI

Harwood JD, et al. Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops. Biol. Control. 2009;51:499–506. doi: 10.1016/j.biocontrol.2009.09.007. DOI

Chailleux, A., Mohl, E. K., Teixeira Alves, M., Messelink, G. J. & Desneux, N. Natural enemy-mediated indirect interactions among prey species: Potential for enhancing biocontrol services in agroecosystems. Pest Manag. Sci.70, 1769–1779 (2014). PubMed

von Berg K, Thies C, Tscharntke T, Scheu S. Cereal aphid control by generalist predators in presence of belowground alternative prey: Complementary predation as affected by prey density. Pedobiologia (Jena). 2009;53:41–48. doi: 10.1016/j.pedobi.2009.03.001. DOI

Mair J, Port GR. Predation by the carabid beetles Pterostichus madidus and Nebria brevicollis is affected by size and condition of the prey slug Deroceras reticulatum. Agric. For. Entomol. 2001;3:99–106. doi: 10.1046/j.1461-9563.2001.00093.x. DOI

Symondson, W. O. C. et al. Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. Bull. Entomol. Res.96, 637–645 (2006). PubMed

Prasad RP, Snyder WE. Polyphagy complicates conservation biological control that targets generalist predators. J. Appl. Ecol. 2006;43:343–352. doi: 10.1111/j.1365-2664.2006.01129.x. DOI

Renkema JM, Lynch DH, Cutler GC, MacKenzie K, Walde SJ. Predation by Pterostichus melanarius (Illiger) (Coleoptera: Carabidae) on immature Rhagoletis mendax Curran (Diptera: Tephritidae) in semi-field and field conditions. Biol. Control. 2012;60:46–53. doi: 10.1016/j.biocontrol.2011.10.004. DOI

Roubinet E, et al. Diet of generalist predators reflects effects of cropping period and farming system on extra- and intraguild prey. Ecol. Appl. 2017;27:1167–1177. doi: 10.1002/eap.1510. PubMed DOI

Honěk A, Saska P, Martinkova Z. Seasonal variation in seed predation by adult carabid beetles. Entomol. Exp. Appl. 2006;118:157–162. doi: 10.1111/j.1570-7458.2006.00376.x. DOI

Talarico F, Giglio A, Pizzolotto R, Brandmayr P. A synthesis of feeding habits and reproduction rhythm in Italian seed-feeding ground beetles (Coleoptera: Carabidae) Eur. J. Entomol. 2016;113:325–336. doi: 10.14411/eje.2016.042. DOI

Charalabidis A, Dechaume-Moncharmont F-X, Carbonne B, Bohan DA, Petit S. Diversity of foraging strategies and responses to predator interference in seed-eating carabid beetles. Basic Appl. Ecol. 2019;36:13–24. doi: 10.1016/j.baae.2019.02.003. DOI

Pilipaviius, V. Weed seed rain dynamics and ecological control ability in agrophytocenosis. in Herbicides—Advances in Research (ed. Price, A.) 51–83 (InTech, 2013). 10.5772/55972.

Saska P, Koprdová S, Martinková Z, Honěk A. Comparing methods of weed seed exposure to predators. Ann. Appl. Biol. 2014;164:301–312. doi: 10.1111/aab.12102. DOI

Johnson NE, Cameron RS. Phytophagous ground beetles. Ann. Entomol. Soc. Am. 1969;62:909–914. doi: 10.1093/aesa/62.4.909. DOI

Russell MC, Lambrinos J, Records E, Ellen G. Seasonal shifts in ground beetle (Coleoptera: Carabidae) species and functional composition maintain prey consumption in Western Oregon agricultural landscapes. Biol. Control. 2017;106:54–63. doi: 10.1016/j.biocontrol.2016.12.008. DOI

Williams CL, et al. Over-winter predation of Abutilon theophrasti and Setaria faberi seeds in arable land. Weed Res. 2009;49:439–447. doi: 10.1111/j.1365-3180.2009.00715.x. DOI

Westerman P, Luijendijk CD, Wevers JDA, Van Der Werf W. Weed seed predation in a phenologically late crop. Weed Res. 2011;51:157–164. doi: 10.1111/j.1365-3180.2010.00834.x. DOI

Winder L, et al. Predatory activity and spatial pattern: The response of generalist carabids to their aphid prey. J. Anim. Ecol. 2005;74:443–454. doi: 10.1111/j.1365-2656.2005.00939.x. DOI

Bohan DA, et al. Spatial dynamics of predation by carabid beetles on slugs. J. Anim. Ecol. 2000;69:367–379. doi: 10.1046/j.1365-2656.2000.00399.x. DOI

Frank SD, Shrewsbury PM, Denno RF. Plant versus prey resources: Influence on omnivore behavior and herbivore suppression. Biol. Control. 2011;57:229–235. doi: 10.1016/j.biocontrol.2011.03.004. DOI

Abrams PA, Matsuda H. Positive indirect effects between prey species that share predators. Ecology. 1996;77:610–616. doi: 10.2307/2265634. DOI

Boetzl FA, Konle A, Krauss J. Aphid cards – Useful model for assessing predation rates or bias prone nonsense? J. Appl. Entomol. 2020;144:74–80. doi: 10.1111/jen.12692. DOI

Bilde T, Toft S. Consumption by carabid beetles of three cereal aphid species relative to other prey types. Entomophaga. 1997;42:21–32. doi: 10.1007/BF02769876. DOI

Madsen M, Terkildsen S, Toft S. Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey. Biocontrol. 2004;49:483–504. doi: 10.1023/B:BICO.0000036442.70171.66. DOI

Fawki, S. & Toft, S. Food preferences and the value of animal food for the carabid beetle Amara similata (Gyll.) (Col., Carabidae). J. Appl. Entomol.129, 551–556 (2005).

Saska P. Effect of diet on the fecundity of three carabid beetles. Physiol. Entomol. 2008;33:188–192. doi: 10.1111/j.1365-3032.2008.00618.x. DOI

Haschek C, Drapela T, Schuller N, Fiedler K, Frank T. Carabid beetle condition, reproduction and density in winter oilseed rape affected by field and landscape parameters. J. Appl. Entomol. 2012;136:665–674. doi: 10.1111/j.1439-0418.2011.01694.x. DOI

Symondson WOC, Sunderland KD, Greenstone MH. Can generalist predators be effective biocontrol agents? Annu. Rev. Entomol. 2002;47:561–594. doi: 10.1146/annurev.ento.47.091201.145240. PubMed DOI

Lundgren, J. G. Chapter 18: Biological control of weed seeds in agriculture using omnivorous insects. in Relationships of Natural Enemies and Non-Prey Foods 333–351 (Springer Netherlands, 2009).

Löbl, I. & Smetana, A. Catalogue of Palaearctic Colcoptera. Vol. 1 (2003).

Homburg, K., Homburg, N., Schäfer, F., Schuldt, A. & Assmann, T. Carabids.org—A dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conserv. Divers.7, 195–205 (2014).

Penell A, Raub F, Höfer H. Estimating biomass from body size of European spiders based on regression models. J. Arachnol. 2018;46:413. doi: 10.1636/JoA-S-17-044.1. DOI

Pey B, et al. A thesaurus for soil invertebrate trait-based approaches. PLoS ONE. 2014;9:e108985. doi: 10.1371/journal.pone.0108985. PubMed DOI PMC

Nentwig, W., Blick, T., Gloor, D., Hänggi, A. & Kropf, C. Araneae: Spiders of Europe. https://araneae.nmbe.ch, https://www.araneae.nmbe.ch (2019).

Caballero M, Baquero E, Ariño AH, Jordana R. Indirect biomass estimations in Collembola. Pedobiologia (Jena). 2004;48:551–557. doi: 10.1016/j.pedobi.2004.06.006. DOI

Migui SM, Lamb RJ. Sources of variation in the interaction between three cereal aphids (Hemiptera: Aphididae) and wheat (Poaceae) Bull. Entomol. Res. 2006;96:235–241. doi: 10.1079/BER2006419. PubMed DOI

Brooks, D. R. et al. Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. I. Soil-surface-active invertebrates. Philos. Trans. R. Soc. B Biol. Sci.358, 1847–1862 (2003). PubMed PMC

Bohan DA, et al. Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape. Proc. R. Soc. B Biol. Sci. 2005;272:463–474. doi: 10.1098/rspb.2004.3049. PubMed DOI PMC

John, F. & Weisberg, S. An R Companion to Applied Regression. (Sage, 2019).

Long, J. jtools: Analysis and Presentation of Social Scientific Data. R package version 2.0.1. (2019).

Lenth, R. emmeans: Estimated Marginal Means, aka Least-Squares Means. (2020).

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

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

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