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      Trust your guts? The effect of gut section on diet composition and impact of Mus musculus on islands using metabarcoding

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          Abstract

          1. DNA metabarcoding is widely used to characterize the diet of species, and it becomes very relevant for biodiversity conservation, allowing the understanding of trophic chains and the impact of invasive species. The need for cost‐effective biodiversity monitoring methods fostered advances in this technique. One question that arises is which sample type provides a better diet representation.

          2. Therefore, with this study, we intended to evaluate if there were differences in diet estimates according to the section of the gastrointestinal tract analysed and which section(s) provided the best diet representation. Additionally, we intended to infer the ecological/economic impacts of an invader as a model of the potential effects in an originally mammal‐free ecosystem.

          3. We examined the gut contents of the house mouse Mus musculus introduced to Cabo Verde, considering three sections: stomach, small intestine, and large intestine. We applied a DNA‐metabarcoding approach using two genetic markers, one specific for plants and another for invertebrates.

          4. We showed that this invader consumed 131 taxa (73 plants and 58 invertebrates). We obtained significant differences in the composition of two of the three sections, with a higher incidence of invertebrates in the stomach and plants in the intestines. This may be due to stomach inhibitors acting on plants and/or to faster absorption of soft‐body invertebrates compared to the plant fibers in the intestines. We verified that the impact of this invader in the ecosystem is predominantly negative, as at least 50% of the ingested items were native, endemic, or economically important taxa, and only 19% of the diet items were exotics.

          5. Overall, results showed the need to analyse only two gastrointestinal tract sections to obtain robust diet data, increasing the cost‐effectiveness of the method. Furthermore, by uncovering the native taxa most frequently preyed on by mice, this DNA‐metabarcoding approach allowed us to evaluate efficiently which are at the highest risk.

          Abstract

          In this article, we assessed the differences in diet estimates and potential ecological and economic impact measurements according to the section of the gastrointestinal tract (stomach, small and large intestine) analysed. We aimed to test which section(s) provided a better diet representation and putative impact of a common inland invader. For that, we examined the gut contents of house mice Mus musculus introduced to Cabo Verde Islands, applying a DNA‐metabarcoding approach. Our results demonstrated that with only two or the three gut sections it is possible to obtain robust diet and impact representations, and that there is a higher incidence of invertebrates in the stomach and of plants in the intestines. In addition, we were able to demonstrate efficiently and with much higher taxonomic resolution than using traditional methods that the impact of this invader is predominantly negative.

          Abstract in Portuguese

          O  metabarcoding de ADN é amplamente utilizado para a caracterização da dieta de espécies, e tornou‐se bastante relevante para a conservação da biodiversidade, permitindo a compreensão sobre cadeias tróficas e o impacto de espécies invasoras. A necessidade de métodos de monitorização da biodiversidade com uma boa relação custo‐benefício fomentaram avanços nesta técnica. Uma questão que se coloca é qual o tipo de amostra que fornece uma melhor representação da dieta. Deste modo, com este estudo, pretendemos avaliar se existem diferenças nas estimativas da dieta de acordo com a secção do tracto gastrointestinal analisada e qual(is) a(s) secção(ões) que proporciona(m) uma melhor representação da dieta. Adicionalmente, pretendemos inferir os impactos ecológicos/ económicos de um invasor como um modelo dos efeitos potenciais que este pode ter num ecossistema originalmente sem mamíferos. Analisámos os conteúdos gastrointestinais do rato doméstico Mus musculus introduzido em Cabo Verde, considerando três secções: estômago, intestino delgado e intestino grosso. Aplicámos uma abordagem de metabarcoding de ADN usando dois marcadores genéticos, um específico para plantas e outro para invertebrados. Mostrámos que este invasor consumiu 131 taxa (73 plantas e 58 invertebrados). Obtivemos diferenças significativas na composição de duas das três secções, com maior incidência de invertebrados no estômago e de plantas nos intestinos. Isto pode dever‐se a inibidores estomacais que agem sobre as plantas e/ ou à absorção mais rápida de invertebrados de corpo mole em comparação com as fibras vegetais nos intestinos. Verificámos que o impacto deste invasor no ecossistema é predominantemente negativo, pois pelo menos 50% dos itens ingeridos eram nativos, endémicos ou economicamente importantes e apenas 19% dos itens da dieta eram exóticos. De modo geral, os resultados mostraram a necessidade de analisar apenas duas secções do tracto gastrointestinal para obter dados robustos da dieta, aumentando a relação custo‐eficácia deste método. Além disso, ao descobrir os taxa nativos mais frequentemente predados por ratos, a abordagem de metabarcoding de ADN permitiu‐nos avaliar com eficiência quais estão sob maior risco.

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          Global biodiversity: indicators of recent declines.

          In 2002, world leaders committed, through the Convention on Biological Diversity, to achieve a significant reduction in the rate of biodiversity loss by 2010. We compiled 31 indicators to report on progress toward this target. Most indicators of the state of biodiversity (covering species' population trends, extinction risk, habitat extent and condition, and community composition) showed declines, with no significant recent reductions in rate, whereas indicators of pressures on biodiversity (including resource consumption, invasive alien species, nitrogen pollution, overexploitation, and climate change impacts) showed increases. Despite some local successes and increasing responses (including extent and biodiversity coverage of protected areas, sustainable forest management, policy responses to invasive alien species, and biodiversity-related aid), the rate of biodiversity loss does not appear to be slowing.
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            Towards next-generation biodiversity assessment using DNA metabarcoding.

            Virtually all empirical ecological studies require species identification during data collection. DNA metabarcoding refers to the automated identification of multiple species from a single bulk sample containing entire organisms or from a single environmental sample containing degraded DNA (soil, water, faeces, etc.). It can be implemented for both modern and ancient environmental samples. The availability of next-generation sequencing platforms and the ecologists' need for high-throughput taxon identification have facilitated the emergence of DNA metabarcoding. The potential power of DNA metabarcoding as it is implemented today is limited mainly by its dependency on PCR and by the considerable investment needed to build comprehensive taxonomic reference libraries. Further developments associated with the impressive progress in DNA sequencing will eliminate the currently required DNA amplification step, and comprehensive taxonomic reference libraries composed of whole organellar genomes and repetitive ribosomal nuclear DNA can be built based on the well-curated DNA extract collections maintained by standardized barcoding initiatives. The near-term future of DNA metabarcoding has an enormous potential to boost data acquisition in biodiversity research. © 2012 Blackwell Publishing Ltd.
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              Mammal invaders on islands: impact, control and control impact

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                Author and article information

                Contributors
                raquel.vasconcelos@cibio.up.pt
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                07 March 2022
                February 2022
                : 12
                : 3 ( doiID: 10.1002/ece3.v12.3 )
                : e8638
                Affiliations
                [ 1 ] CIBIO Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Campus de Vairão, Universidade do Porto Vairão Portugal
                [ 2 ] Departamento de Biologia Faculdade de Ciências da Universidade do Porto Porto Portugal
                [ 3 ] BIOPOLIS Program in Genomics, Biodiversity and Land Planning CIBIO, Campus de Vairão Vairão Portugal
                [ 4 ] ISECMAR‐UTA Instituto Engenharia e Ciências do Mar da Universidade Técnica do Atlântico Mindelo Cabo Verde
                [ 5 ] INIDA Instituto Nacional de Investigação e Desenvolvimento Agrário Santiago Cabo Verde
                [ 6 ] LEAF‐ISA Linking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia Universidade de Lisboa Lisboa Portugal
                Author notes
                [*] [* ] Correspondence

                Raquel Vasconcelos, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado Campus de Vairão, Universidade do Porto, 4485‐661 Vairão, Portugal

                Email: raquel.vasconcelos@ 123456cibio.up.pt

                Author information
                https://orcid.org/0000-0003-0353-7885
                https://orcid.org/0000-0003-3938-1560
                https://orcid.org/0000-0003-2569-0768
                https://orcid.org/0000-0002-7423-119X
                https://orcid.org/0000-0002-9373-6302
                https://orcid.org/0000-0002-4717-9429
                Article
                ECE38638
                10.1002/ece3.8638
                8901889
                35309743
                1b0397ac-ed65-4f8d-af8d-90da712a72fd
                © 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 January 2022
                : 06 August 2021
                : 27 January 2022
                Page count
                Figures: 5, Tables: 1, Pages: 0, Words: 12570
                Funding
                Funded by: LEAF: Linking Landscape, Environment, Agriculture and Food Research Centre
                Award ID: UIDB/04129/2020
                Funded by: Gabinete de Ensino Superior, Ciência e Tecnologia do Ministério da Educação, Governo de Cabo Verde
                Funded by: Aga Khan Foundation , doi 10.13039/100004448;
                Award ID: CVAgrobiodiversity/333111699
                Funded by: Fundação para a Ciência e a Tecnologia , doi 10.13039/501100001871;
                Award ID: DL57/2016/CP1440/CT0002
                Award ID: SFRH/BD/145851/2019
                Funded by: Norte Portugal Regional Operational Programme (NORTE2020)
                Award ID: NORTE‐01‐0145‐FEDER‐000046
                Funded by: Horizon 2020 Framework Programme , doi 10.13039/100010661;
                Award ID: 668981
                Funded by: Instituto de Ciências e Tecnologias Agrárias e Agro‐Alimentares da Universidade do Porto (ICETA)
                Award ID: ICETA 2016‐31
                Categories
                Agroecology
                Applied Ecology
                Biodiversity Ecology
                Botany
                Conservation Ecology
                Entomology
                Genetics
                Invasion Ecology
                Zoology
                Research Article
                Research Articles
                Custom metadata
                2.0
                February 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.1.2 mode:remove_FC converted:10.03.2022

                Evolutionary Biology
                cabo verde islands,diet,gastrointestinal tract,house mouse,invasive species,invertebrates,next‐generation sequencing,plants

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