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Species‐Level Ichthyoplankton Dynamics for 97

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Species‐Level Ichthyoplankton Dynamics for 97 Received: 16 October 2020 | Revised: 20 February 2021 | Accepted: 23 April 2021 DOI: 10.1111/mec.15944 ORIGINAL ARTICLE Species- level ichthyoplankton dynamics for 97 fishes in two major river basins of the Amazon using quantitative metabarcoding Cédric Mariac1,2 | Jean- François Renno1,2 | Carmen Garcia- Davila2,3 | Yves Vigouroux1,2 | Eduardo Mejia2,3 | Carlos Angulo2,3 | Diana Castro Ruiz2,3 | Guillain Estivals2,3 | Christian Nolorbe2,3 | Aurea García Vasquez2,3 | Jesus Nuñez2,4 | Gérard Cochonneau5 | Mayra Flores2,3 | Jhon Alvarado2,3 | José Vertiz2,3 | Werner Chota- Macuyama2,3 | Homero Sánchez2,3 | Guido Miranda2,6,7 | Fabrice Duponchelle2,8 1DIADE, Univ Montpellier, CIRAD, IRD, Montpellier, France Abstract 2Laboratoire Mixte International The Amazon basin holds the world's largest freshwater fish diversity. Information on - Evolution et Domestication de l’Ichtyofaune Amazonienne (LMI - EDIA), the intensity and timing of reproductive ecology of Amazonian fish is scant. We use IIAP, UAGRM, IRD, Montpellier, France a metabarcoding method by capture using a single probe to quantify species- level 3 Laboratorio de Biología y Genética ichthyoplankton dynamics. We sampled the Marañón and the Ucayali rivers in Peru Molecular (LBGM), Instituto de Investigaciones de la Amazonía Peruana monthly for 2 years. We identified 97 species that spawned mainly during the flood (IIAP), Iquitos, Perú start, the flood end or the receding periods, although some species had spawning ac- 4BOREA, MNHN, SU, UA, CNRS, IRD, tivity in more than one period. This information was new for 40 of the species in the Université de Caen- Normandie, France 5GET, CNRS, IRD, Université de Toulouse, Amazon basin and 80 species in Peru. Most species ceased spawning for a month dur- Toulouse, France ing a strong hydrological anomaly in January 2016, demonstrating the rapidity with 6 Wildlife Conservation Society, Bolivia which they react to environmental modifications during the breeding season. We also Program, La Paz, Bolivia 7Unidad de Limnología, Instituto de document another unreported event in the Amazon basin, the inverse phenology of Ecología, Universidad Mayor de San species belonging to one genus (Triportheus). Overall larval flow in the Marañón was Andrés, La Paz, Bolivia more than twice that of the Ucayali, including for most commercial species (between 8MARBEC, CNRS, Ifremer, IRD, Univ Montpellier, Montpellier, France two and 20 times higher), whereas the Ucayali accounts for ~80% of the fisheries landings in the region. Our results are discussed in the light of the main anthropo- Correspondence Cédric Mariac, DIADE, Univ Montpellier, genic threats to fishes, hydropower dam construction and the Hidrovía Amazónica, CIRAD, IRD, Montpellier, France. and should serve as a pre- impact baseline. Email: [email protected] Funding information KEYWORDS Concejo Nacional de Ciencia y Tecnología capture, fish larvae, Marañón, metabarcoding, phenology, Ucayali (CONCYTEC), Grant/Award Number: 0 8 8 - 2 0 1 4 - FONDECYT- DE †This study is dedicated to the memory of Aurea Garcia Vasquez, dearest colleague and friend who succumbed to covid- 19. We miss you. Molecular Ecology. 2021;00:1–22. wileyonlinelibrary.com/journal/mec © 2021 John Wiley & Sons Ltd | 1 2 | MARIAC ET AL. 1 | INTRODUCTION et al., 2016; Maggia et al., 2017; Wilcox et al., 2018). Although these methods have proved very useful and cost- effective on a qualitative The Amazon basin is the most species- rich ecosystem on Earth. basis, there have been many doubts about whether they could pro- Its extensive river network holds ~16% of the world's surface, liq- vide reliable quantitative results, especially with PCR- based meth- uid fresh waters (Latrubesse et al., 2017) and provides ~20% of the ods owing to amplification biases, barcode chimeras, and a level of world's freshwater discharge (Salati & Vose, 1984). It also hosts the bias depending on the primers used and the number of PCR cycles world highest freshwater fish diversity, with 2,406 described spe- (Duke & Burton, 2020; Lamb et al., 2019; Piñol et al., 2019; Zinger cies, which represents 15% of the world's freshwater fishes (Jézéquel et al., 2019). Another approach, using shotgun metagenomics, suc- et al., 2020). Once relatively pristine, the Amazon basin is now facing cessfully generated quantitative species- level estimates of larval increasing threats from growing human activities and climate change abundance on coral reef fishes in the Red Sea (Kimmerling et al., and is considered in transition to a disturbance- dominated regime 2018). For Amazonian fish species, we recently proposed a new (Davidson et al., 2012). Fresh waters are the most degraded and im- method based on hybridization capture of the COI gene using a sin- perilled ecosystems in the world (Carpenter et al., 2011; Dudgeon gle, almost universal probe from a species absent from the Amazon et al., 2006; Vörösmarty et al., 2010) and freshwater fishes are basin and approximately genetically equidistant from all Amazonian among the most threatened vertebrates in the world (Pimm et al., fish species (Mariac et al., 2018). This new metabarcoding by capture 2014). This also holds true in the Amazon basin, where the drivers of using a single probe (MCSP) methodology showed strong correla- aquatic ecosystem degradation and threats to fishes are mostly the tions with true frequencies estimated by a Sanger approach, allow- same as those threatening freshwater biodiversity worldwide: over- ing the development of a reliable quantitative approach. exploitation, flow modification by dams, deforestation, destruction Here, we use this method to quantify and compare, over two or degradation of habitat, water pollution, invasion by exotic species consecutive hydrological cycles, the species- level fish larval dynam- and climate change (Castello & Macedo, 2016; Castello et al., 2013). ics in two of the most important tributaries of the Peruvian Amazon, Beside their exceptional diversity, fish represent the main the Marañón and Ucayali rivers. Besides overharvesting problems source of animal protein for people of the Amazon basin, with common to most highly populated Amazonian regions (Castello some of the world's highest fish consumption rates per capita (up et al., 2013), the ichthyofauna of these two rivers is also threatened to 200 kg year−−1 for rural populations, (Batista et al., 1998; Isaac & by planned anthropogenic activities such as the building of dams and Almeida, 2011). The rapidly growing human Amazonian population waterways (Anderson et al., 2018; Bodmer et al., 2018). We sampled (a 10- fold increase between 1960 and 2010 in Brazil alone, from 2.5 larvae monthly during two consecutive annual cycles in fixed locali- to 24.3 million; DeFries et al., 2010; Tritsch & Le Tourneau, 2016) ties just upstream of the confluence of the Marañón and Ucayli riv- is exerting increasing pressure on natural resources and on fishes ers to answer the following research questions: What is the diversity in particular. Most large, highly valued species are already overex- of fish species spawning in the main channels of the Marañón and ploited in the Amazon basin and have been progressively replaced Ucayali? What are their spawning periods and relative abundance in by smaller, less- prized species with faster turnover rates (Castello relation to the hydrological cycle? What is the relative contribution et al., 2013). Yet, basic life history information on the reproductive of these two rivers to the production of commercial fish larvae? periods, spawning grounds and larval recruitment of many exploited species, which are crucial determinants of fish reproductive success in an ecosystem, are often lacking for proposing sustainable fisher- 2 | METHODS ies management practices and conservation strategies. Traditional approaches that consist of monitoring adult populations over a com- 2.1 | Study area and sampling plete annual cycle, at least, can be so costly and time- consuming on many species or on large, highly valued and rare species, as to Between January 2015 and December 2016, fish larvae (ichthyo- become unrealistic. Obtaining this information by sampling their plankton) were sampled monthly at the same localities in two eggs and larvae could be an interesting alternative solution now that tributaries of the Amazon River: the Ucayali and Marañón in Peru. advances in molecular techniques, such as barcoding, have solved Both the Marañón and Ucalayi rivers are white water rivers origi- the long- standing problems of taxonomic identification of early life nating in the Andes. At their confluence they form the Amazonas stages (Becker et al., 2015; Frantine- Silva et al., 2015; García Dávila River. Both have beds mainly made up of sandy, silty and clayey et al., 2015). Obtaining individual barcodes for each egg or larvae, sediments but the Ucayali is much more dynamic in its formation however, can quickly become cost- ineffective and time- consuming, of meanders and channels than the Marañón. According to the and then unrealistic when large numbers of larvae are involved SO- HYBAM data set (www.so- hybam.org), during the two years of (Evans et al., 2016). Taking advantage of next generation sequencing study (2015 and 2016) the average flow was 17.9 m3 s– 1 (CV =0.34) (NGS), metabarcoding approaches allowing the massive sequencing in Marañón River, 11.7 m3 s– 1 (CV =0.51) in the Ucayali River, with of large numbers of larvae in bulk have recently emerged, using ei- averaged current velocities of 1.51 m s– 1 (CV =0.18) and 1.16 m s– 1 ther polymerase chain reaction (PCR)- based (Loh et al., 2014; Nobile (CV =0.34), respectively. The two rivers have a marked and similar et al., 2019) or capture- based methods (Gauthier et al., 2020; S. Liu seasonality with a flooding (October to April) and a receding phase MARIAC ET AL. | 3 PongodeManseriche Hydrological stations damproject FIGURE 1 Map of the Amazon basin with a close- up on the study area in the Peruvian Amazon, illustrating the main cities (black squares) and the monthly sampling locations (red dots) in the Marañón and Ucayali rivers.
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