DNA metabarcoding of gut contents reveals natural predation by spiders on Xylella fastidiosa vectors in the southwestern Spain agroecosystem

Laura Avivar-Lozano; José M. Molina; Sergio Pérez-Guerrero

doi:10.5424/sjar/2024224-20842

Laura Avivar-Lozano Laboratorio de Entomología. IFAPA. Centro “Las Torres”. Crta. Sevilla-Cazalla de la Sierra, Km 12,2. 41200 Alcalá del Río (Sevilla). Spain https://orcid.org/0000-0002-3932-1990
José M. Molina Laboratorio de Entomología. IFAPA. Centro “Las Torres”. Crta. Sevilla-Cazalla de la Sierra, Km 12,2. 41200 Alcalá del Río (Sevilla). Spain https://orcid.org/0000-0001-5841-7368
Sergio Pérez-Guerrero Laboratorio de Entomología. IFAPA. Centro “Las Torres”. Crta. Sevilla-Cazalla de la Sierra, Km 12,2. 41200 Alcalá del Río (Sevilla). Spain https://orcid.org/0000-0002-3098-9978

DOI: https://doi.org/10.5424/sjar/2024224-20842

Palabras clave: control natural, Araneae, Aphrophoridae, olivar, cítricos, vid

Resumen

Objetivo de estudio: Dilucidar qué especies y gremios de arañas depredan sobre los vectores de Xylella fastidiosa en agroecosistemas del suroeste de España empleando técnicas de secuenciación masiva.

Área de estudio: Suroeste de España.

Material y métodos: El muestreo de arañas se realizó sobre la cobertura vegetal asociada a cultivos de olivar, cítricos y vid usando un aspirador de batería. El ADN se aisló de cada muestra utilizando el kit E.Z.N.A.® Tissue DNA (Omega Bio-tek). Se diseñó un par de cebadores para amplificar el ADN específico de las presas potenciales de las arañas pertenecientes al orden Hemiptera: Philaenus spumarius, Neophilaenus campestris, Neophilaenus lineatus, Lepyronia coleoptrata, Aphrophora spp., Cicadella viridis y Cercopis spp. La asignación taxonómica se realizó utilizando la base de datos de referencia MetaCOXI, basada en European Nucleotide Archive (ENA) y Barcode of Life Data System (BOLD).

Resultados principales: Neophilaenus campestris fue detectado en dos especies de arañas: Enoplognatha caricis (Theridiidae) y Thanatus vulgaris (Philodromidae) (10.4% de los especímenes capturados). Además, L. coleoptrata fue depredada por Haplodrassus macellinus (Gnaphosidae) (3.5%). No se encontró ADN de P. spumarius en ninguna de las muestras. Hubo depredación sobre Aphrophoridae en todos los cultivos excepto en olivar. Finalmente, los gremios de arañas “otras cazadoras”, “cazadoras terrestres” y formadoras de “telas aéreas espaciales” depredaron sobre Aphrophoridae.

Aspectos destacados de la investigación: Algunas especies de arañas encontradas en los viñedos (50% de los especímenes capturados) consumieron N. campestris.

Descargas

La descarga de datos todavía no está disponible.

Citas

Balech B, Sandioniggi A, Marzano M, Pesole G, Santamaria M, 2022. MetaCOXI: An integrated collection of metazoan mitochondrial cytochrome oxidase subunit-i DNA sequences. Database 11, 1918. https://doi.org/10.1093/database/baab084

Barrientos, JA, 2006. Claves de los arácnidos ibéricos (documento de trabajo). Jornadas sobre taxonomía de arácnidos ibéricos. III Curso Práctico de Aracnología, Grupo Ibérico de Aracnología, Córdoba 20 al 24 de julio, 198 pp.

Benhadi-Marín J, Villa M, Pereira LF, Rodrigues I, Morente M, Baptista P, Pereira JA, 2020. A guild-based protocol to target potential natural enemies of Philaenus spumarius (Hemiptera: Aphrophoridae), a vector of Xylella fastidiosa (Xanthomonadaceae): A case study with spiders in the olive grove. Insects. 3; 11(2): 100. https://doi.org/10.3390/insects11020100

Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J, 2018. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2's q2-feature-classifier plugin. Microbiome 6: 90. https://doi.org/10.1186/s40168-018-0470-z

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL, 2009. BLAST+: architecture and applications. BMC Bioinformatics 10: 421. https://doi.org/10.1186/1471-2105-10-421

Cárdenas M, Castro J, Campos M, 2012. Short-term response of soil spiders to cover-crop removal in an organic olive orchard in a Mediterranean setting. J Insect Sci. 12: 61. https://doi.org/10.1673/031.012.6101

Cavalieri V, Altamura G, Fumarola G, di Carolo M, Saponari M, Cornara D, Bosco D, Dongiovanni C, 2019. Transmission of Xylella fastidiosa subspecies pauca sequence type 53 by different insect species. Insects 10(10): 324. https://doi.org/10.3390/insects10100324

Deagle BE, Thomas AC, McInnes JC, Clarke LJ, Vesterinen EJ, Clare EL, Kartzinel TR, Eveson JP, 2019. Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? Mol Ecol. 28(2): 391-406. https://doi.org/10.1111/mec.14734

Greco C, Kevan P, 1999. Polyethism in foraging in a polymorphic predator, Enoplognatha ovata (Araneae: Theridiidae): a case for balance. Can Entomol 131(2): 259-268. https://doi.org/10.4039/Ent131259-2

Hambäck PA, Cirtwill AR, García D, Grudzinska-Sterno M, Miñarro M, Tasin M, Yang X, Samnegård, U, 2021. More intraguild prey than pest species in arachnid diets may compromise biological control in apple orchards. Basic Appl Ecol 57: 1-13. https://doi.org/10.1016/j.baae.2021.09.006

Harper G, Whittaker J, 1976. The role of natural enemies in the colour polymorphism of Philaenus spumarius (L.). J. Anim. Ecol. 45,91-104. https://doi.org/10.2307/3769

Hartig F, 2022. DHARMa: Residual diagnostics for hierarchical (Multi-Level / Mixed) regression models. R package version 0.4.6. https://CRAN.R-project.org/package=DHARMa [11 July 2023].

Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S, 2023. multcomp: Simultaneous Inference in General Parametric Models. https://cran.r-project.org/web/packages/multcomp/index.html [11 July 2023].

Illumina, 2017. Effects of Index Misassignment on Multiplexing and Downstream Analysis. 4pp. https://www.illumina.com/content/dam/illumina-marketing/documents/products/whitepapers/index-hopping-white-paper-770-2017-004.pdf.

Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V, Boehm JT, Machida RJ, 2013. A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: Application for characterizing coral reef fish gut contents. Front Zool 10: 1-14. https://doi.org/10.1186/1742-9994-10-34

Liccardo A, Fierro A, Garganese F, Picciotti U, Porcelli F, 2020. A biological control model to manage the vector and the infection of Xylella fastidiosa on olive trees. PLoS One 15(4): e0232363. https://doi.org/10.1371/journal.pone.0232363

Liu M, Clarke LJ, Baker SC, Jordan GJ, Burridge CP, 2020. A practical guide to DNA metabarcoding for entomological ecologists. Ecological Entomology (2020), 45: 373-385. https://doi.org/10.1111/een.12831

Marc P, Canard A, Ysnel F, 1999. Spiders (Araneae) useful for pest limitation and bioindication. Agric Ecosyst Environ. 74: 229-273. https://doi.org/10.1016/B978-0-444-50019-9.50015-7

Michalko R, Pekár, S, Entling MH, 2019. An updated perspective on spiders as generalist predators in biological control. Oecologia 189: 21-36. https://doi.org/10.1007/s00442-018-4313-1

Morelli M, García-Madero JM, Jos A, Saldarelli P, Dongiovanni C, Kovacova M, Saponari M, Baños Arjona A, Hackl E, Webb E, Compant S, 2021. Xylella fastidiosa in olive: A review of control attempts and current management. Microorganisms 9(8): 1771. https://doi.org/10.3390/microorganisms9081771

Morris TI, Symondson W, Kid N, Campos M, 1999. Las arañas y su incidencia sobre Prays oleae en el olivar. Boletín Sanidad Vegetal Plagas 25: 475-489.

Ortiz D, Petrakova L, Pekar S, 2021. Gut content metabarcoding of three widespread Iberian ant-eating spiders reveals specialisation on the same abundant harvester ants. Ecol Entomol. 47(3): 305-313. https://doi.org/10.1111/een.13114

Phillipson J, 1960. A contribution to the feeding biology of Mitopus morio (F) (Phalangida). J. Anim. Ecol. 29: 35-43. https://doi.org/10.2307/2269

R Core Team, 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Redak RA, Purcell AH, Lopes JR, Blua MJ, Mizell III, RF, Andersen PC, 2004. The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu Rev Entomol 49: 243-270. https://doi.org/10.1146/annurev.ento.49.061802.123403

Rodrigues I, Ramos V, Benhadi-Marín J, Moreno A, Fereres A, Pereira JA, Baptista P, 2022. A novel molecular diagnostic method for the gut content analysis of Philaenus DNA. Sci Rep. 12(1): 492. https://doi.org/10.1038/s41598-021-04422-1

Rosas-Ramos N, Baños-Picón L, Tobajas E, de Paz V, Tormos J, Asís JD, 2018. Value of ecological infrastructure diversity in the maintenance of spider assemblages: a case study of mediterranean vineyard agroecosystems. Agric Ecosyst Env 265: 244-253. https://doi.org/10.1016/j.agee.2018.06.026

Saponari M, Boscia D, Nigro F, Martelli GP, 2013. Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (southern Italy). J Plant Pathol 95: 659-668.

Saponari M, Loconsole G, Cornara D, Yokomi RH, De Stradis A, Boscia D, Bosco D, Martelli GP, Krugner R, Porcelli F, 2014. Infectivity and transmission of Xylella fastidiosa Salento strain by Philaenus spumarius L., (Hemiptera: Aphrophoridae) in Puglia, Italy. J Econ Entomol 107: 1316-1319. https://doi.org/10.1603/EC14142

Saqib, HSA, Liang, P, You, M, Gurr, GM, 2021. Molecular gut content analysis indicates the inter- and intra-guild predation patterns of spiders in conventionally managed vegetable fields. Ecol. Evol. 11: 9543-9552. https://doi.org/10.1002/ece3.7772

Serio F, Imbriani G, Girelli CR, Miglietta PP, Scortichini M, Fanizzi FP, 2024. A Decade after the Outbreak of Xylella fastidiosa subsp. pauca in Apulia (Southern Italy): Methodical Literature Analysis of Research Strategies. Plants 13(11): 1433. https://doi.org/10.3390/plants13111433

Uetz, GW, 1992. Foraging strategies of spiders. Trends Ecol Evol 7: 155-159. https://doi.org/10.1016/0169-5347(92)90209-T

Uiterwaal SF, DeLong JP, 2020. Using patterns in prey DNA digestion rates to quantify predator diets. Mol Ecol Resour 20(6): 1723-1732. https://doi.org/10.1111/1755-0998.13231

Val Nolan, Jr, 1956. Spittle Insects as Food of Prairie Warblers. The Auk, 73(4): 557. https://doi.org/10.2307/4081955

Whittaker JB,1970. Cercopid spittle as microhabitat. Oikos 21: 59-64. https://doi.org/10.2307/3543839