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Metabarcoding, Direct Stomach Observation and Stable Isotope bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.249896; this version posted May 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 1 Title: 2 3 2 Metabarcoding, direct stomach observation and stable isotope analysis reveal a highly 4 5 6 3 diverse diet for the invasive green crab in Atlantic Patagonia 7 8 4 9 10 11 5 Authors-- 12 13 6 Georgina Cordone1, Mariana Lozada 2, Elisabet Vilacoba 3, Bettina Thalinger 4,5, Gregorio Bigatti 6,7, 14 15 3 4,5 1 16 7 Darío A. Lijtmaer , Dirk Steinke , David E. Galván * 17 18 8 19 20 9 * Corresponding author: [email protected] ; Tel: +54 (280) 488-3184 Ext. 1277 - Fax: 21 22 10 +54 (280) 488-3543 23 11 24 25 12 26 27 1 28 13 Centro para el Estudio de Sistemas Marinos (CESIMAR), Consejo Nacional de Investigaciones 29 30 14 Científicas y Técnicas (CONICET), Edificio CCT CONICET-CENPAT, Bvd. Brown 2915, 31 32 33 15 (U9120) Puerto Madryn, Chubut, Argentina. 34 35 16 2 Laboratorio de Microbiología Ambiental (IBIOMAR), Consejo Nacional de Investigaciones 36 37 38 17 Científicas y Técnicas (CONICET), Edificio CCT CONICET-CENPAT, Bvd. Brown 2915, 39 40 18 (U9120) Puerto Madryn, Chubut, Argentina. 41 42 19 3 División Ornitología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” MACN- 43 44 45 20 CONICET. Av. Ángel Gallardo 470 (C1405) Ciudad Autónoma de Buenos Aires, Buenos Aires, 46 47 21 Argentina. 48 49 4 50 22 Centre for Biodiversity Genomics,University of Guelph, 50 Stone Rd E (N1G2W1), Guelph, 51 52 23 Ontario, Canada. 53 54 5 55 24 Department of Integrative Biology, College of Biological Science, University of Guelph, 50 Stone 56 57 25 Rd E (N1G 2W1), Guelph, Ontario, Canada. 58 59 26 6 Laboratorio de Reproducción y Biología Integrativa de Invertebrados Marinos, (LARBIM, 60 61 62 27 IBIOMAR). Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Edificio 63 64 65 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.249896; this version posted May 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 28 CCT CONICET-CENPAT, Bvd. Brown 2915, (U9120) Puerto Madryn, Chubut, Argentina. 2 3 29 7 Universidad Espíritu Santo, Ecuador 4 5 6 7 30 Declarations 8 9 10 31 Acknowledgements 11 12 13 14 32 We would like to thank Florencia Ríos, Manuela Funes, Juan Pablo Livore, and Maria 15 16 33 Martha Mendez for their fieldwork support. We would like to thank Agustina Ferrando, Cynthia 17 18 19 34 Ibarra, Pablo Macchi and, German Cheli for expert assessment on taxonomic identifications. We are 20 21 35 grateful to two anonymous reviewers for their constructive feedback on the original manuscript 22 23 24 36 version. 25 26 27 37 Funding 28 29 30 31 38 This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas 32 33 39 (CONICET, Argentina) and Sistema Nacional de Datos Genómicos (SNDG, Argentina). Fieldwork 34 35 36 40 campaigns and stable isotope analysis were funded by Fondo para la Investigación Científica y 37 38 41 Tecnológica (FonCyT) under the grants PICT 2017-2403, PICT 2018-0903 and PICT 2018-0969. 39 40 42 The metabarcoding analysis was funded by the Natural Sciences and Engineering Research Council 41 42 43 43 of Canada and the Canada First Research Excellence Fund. 44 45 46 44 Conflicts of interest 47 48 49 50 45 The authors declare that they have no conflict of interest. 51 52 53 46 Ethical approval 54 55 56 57 47 All applicable institutional and/or national guidelines for the care and use of animals were 58 59 48 followed. Permissions for sample collection were granted from the Secretaría de Pesca and 60 61 62 49 Secretaría de Conservación de Áreas Protegidas from Chubut Province. Exportation permissions 63 64 50 were granted in 2019 by the Dirección Nacional de Biodiversidad (Secretaría de Ambiente y 65 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.249896; this version posted May 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 51 Desarrollo Sustentable) under ANEXO II, resolution number: IF-2019-40388897-APN- 2 3 52 DNBI#SGP. 4 5 6 7 53 Consent to participate 8 9 10 54 Not applicable 11 12 13 14 55 Consent for publication 15 16 17 56 Not applicable 18 19 20 21 57 Availability of data and material 22 23 24 58 All data generated and analysed during this study are included in Electronic Supplementary 25 26 27 59 Material: Online Resource 1, 2, 3, 4, and 5 (ESM 1, ESM 2, ESM 3, ESM 4, ESM 5, and ESM 6). 28 29 60 The sequence raw data has been uploaded to Genbank SRA (accession: SRR13517441). 30 31 32 33 61 Code availability 34 35 36 62 The code was implemented in R and it is available under request (R Core Team, 2020). 37 38 39 40 63 Author Contributions 41 42 43 64 DEG, GB, ML, and GC conceived and designed this study. DEG, GB, and GC took the 44 45 46 65 samples. GC conducted the visual analysis and prepared the samples for stable isotope analysis. GC 47 48 66 and DEG analyzed direct stomach observation and stable isotope data. ML contributed to preparing 49 50 51 67 the metabarcoding samples and analyzed metabarcoding data. EV visited as an invited researcher 52 53 68 the Centre for Biodiversity Genomics to obtain the metabarcoding data. EV, BT, DAL, and DS 54 55 69 contributed to the generation of metabarcoding data, molecular and bioinformatic analyses. All 56 57 58 70 authors contributed to manuscript writing. 59 60 61 62 63 64 65 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.249896; this version posted May 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 71 Abstract 2 3 72 The European green crab Carcinus maenas and its sister species C. aestuarii are highly 4 5 6 73 invasive species causing damage to coastal ecosystems and severe economic losses worldwide. C. 7 8 74 maenas was first detected at the Atlantic Patagonian coast in 2001. In this work, we studied the diet 9 10 11 75 of the green crab in a recently invaded location in Golfo Nuevo, using three complementary 12 13 76 techniques: direct stomach observation, metabarcoding of the gut content and stable isotope 14 15 16 77 analysis. Direct stomach observation and metabarcoding showed that green crabs have a broad 17 18 78 omnivorous diet, ingesting most of the phyla present in the study area. Gut content metabarcoding 19 20 79 allowed a detailed description of algae diversity and revealed other taxa that went unnoticed in the 21 22 23 80 visual stomach analysis. Stable isotope analysis showed that the major contribution to crabs' diet 24 25 81 was from the phytoplankton chain (by bivalve consumption) and not directly from algae. This study 26 27 28 82 approach combining three complementary techniques also allowed us to detect some differences in 29 30 83 the diet between sexes, which suggests that male and female crabs are not as ecologically equivalent 31 32 33 84 as previously thought. Besides, we detected sequences corresponding to C. aestuarii suggesting that 34 35 85 the green crab Patagonian population is a hybrid of both sister species. These findings are key to 36 37 38 86 understanding the impacts green crabs could trigger on the local ecosystem. 39 40 87 41 42 88 Keywords: Carcinus maenas, Carcinus aestuarii, e-DNA, Rocky shore ecology, Trophic 43 44 45 89 interactions 46 47 90 48 49 50 91 1. Introduction 51 52 53 92 Invasive species, particularly invasive predators are one of the main causes of worldwide 54 55 56 93 species decline and biodiversity loss (Clavero and García-Berthou 2005; Doherty et al. 2016). Once 57 58 94 invasive species arrive at a new location, they establish new ecological interactions with resident 59 60 61 95 species and these new interactions can have positive or negative effects on native species or the 62 63 96 entire native food web (David et al. 2017). The ways biological invasions impact food webs are 64 65 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.13.249896; this version posted May 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 97 complex and context-dependent as there are various direct and indirect mechanisms by which an 2 3 98 invasive species can affect other taxa (Thomsen et al. 2011a, b).
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