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    Monthly spatial dynamics of the Bay of Biscay hake-sole-Norway lobster fishery: an ISIS-Fish database

    We took as a starting point the hake – sole – Norway lobster Bay of Biscay ISIS-Fish database used for COSELMAR project16,20 (see http://isis-fish.org/download.html section “Bay of Biscay scenario dataset”, Database V0 in Fig. 1). This database was built using 2010 data, and was not calibrated, as it was designed for a geo-foresight study. Since our aim was to describe the system over a decade and simulate realistic dynamics close to available observations to assess management measures, we needed to update the parametrisation and calibrate the database. We took 2010–2012 as the calibration period, and 2013–2020 as the simulation period (grey arrow Fig. 1). The database has a monthly temporal resolution (constrained by the ISIS-Fish framework) and the spatial scale was set to match ICES statistical rectangles (0.5° latitude by 1° longitude rectangles, defined by the International Council for the Exploration of the Sea (ICES) https://www.ices.dk/data/maps/Pages/ICES-statistical-rectangles.aspx), consistent with available knowledge and data.In this section, we firstly describe all the data sources used to update and calibrate the database. Then, for each main component of an ISIS-Fish database – i.e. populations, exploitation and management – we describe this paper’s database parameters and assumptions. We finally describe the calibration procedure (inspired by previous work21,22), of which some results are shown in the Technical Validation section. We summarized this workflow in Fig. 1.Data sourcesData sources, estimates, and literature (including grey literature) were needed to update and calibrate the model. They are marked in Fig. 1 with salmon (data sources and estimates) and mustard (literature) blocks:

    SACROIS23: French landings and effort logbook declarations for 2010 were made available at the log-event*commercial category*ICES statistical rectangle*population scale. It was used to design exploitation features of the database, as well as populations spatial structure.

    LANGOLF survey: 2006–2010 LANGOLF surveys observations for 2006–2010 were made available for Norway lobster. They were used to work on Norway lobster abundance per length class and sex.

    Intercatch: catch observations for 2010–2020 in the Bay of Biscay for hake, at the quarter-métier group scale, and catch observations per class for sole on 2010–2012, and 2010 Norway lobster catch observations per sex and length class24, used to describe the inter-annual effort dynamics, to calibrate and validate the model.

    Estimates of hake abundance per size class in 2010, and hake quarterly estimates of recruitment on 2010–2012 from a northern hake spatial stock assessment model21, used to inform hake biology assumptions (named Other 1 in Fig. 1).

    ICES WGBIE24 2010 estimates of abundance per class (sole and Norway lobster), to inform their abundance at the initial time step; 2010–2012 yearly fishing mortality estimates per age class (sole) to calibrate the database (named Other 2 in Fig. 1).

    Other population, exploitation and management assumptions were informed with scientific literature25 and grey literature26,27 (Literature block in Fig. 1).

    Management assumptions were informed with legal texts2,4,28,29,30,31,32,33,34 and reported quota values in working group reports24.

    About populationsThis section describes for each species the assumptions and parameters values, except for accessibility, which has been calibrated, as described in section Calibration procedure. For all assumptions and values, more details are provided in Supplementary Information’s section 2.2.HakeThe stock size structure was defined with 1 cm size bins for [1;40[cm individuals, 2 cm for [40;100[cm individuals, and 10 cm for [100;130+] cm individuals35. Areas of presence were defined based on 2010 SACROIS French landings data per commercial category and statistical rectangle23, leading to the definition of a presence, a recruitment, an interim recruitment and a spawning area25 (see Supplementary Information’s section 2.2 and Figure S1). These areas allow for the description of intra-Bay of Biscay migrations related to spawning and recruitment processes: mature individuals aggregate at the beginning of the year on the shelf break to spawn, and then disperse on the shelf36,37,38,39,40 (at the beginning of April and July in the model). Also, from age 1 (around 20 cm), individuals in recruitment zone spread in interim recruitment zone, to model a diffusion towards areas neighbouring the nursery area, at the beginning of each time step (see Supplementary Information’s section 2.2 and Table S11). Maturity-at-size and weight-at-length relationships were the same functions as used by ICES working group35,41. Natural mortality was fixed at 0.5, basing on preliminar runs, instead of the commonly used 0.442. Recruitment values were defined prior to the simulation for 2010–2020 using available estimates on the 2010–2015 time series21,27. Deterministic estimates from these sources were allocated to the recruitment area in the Bay of Biscay and the beginning of each month in January-September on the whole time series, of which values are provided in the Supplementary Information’s section 2.2 and Table S3. Growth is modelled through monthly growth increments5,25. However, given the different widths of size bins in the implemented size structure, a correction was provided to values in the transition matrix to eliminate artifacts when growing to a size bin wider than the size bin of origin, as detailed in Supplementary Information’s section 2.2. Abundance at the initial step in each zone was estimated from Bay of Biscay abundance estimates for 201021. Mature individuals over 20 cm were allocated to the spawning area, all individuals strictly shorter than 20 cm were allocated to the recruitment area (as they were assumed to be less than 1 year old), and remaining individuals were allocated to the interim recruitment area. None were allocated to the presence area, in which individuals will go later in the time series, after disaggregating from the spawning area25 (Table S13).SoleThe stock is age structured, with 7 classes going from ages 2 to 7+43 (Table S2). No seasonal variations were implemented. Only a single presence zone was defined (see Supplementary Information’s section 2.2 and Figure S1), as in preliminary runs defining more presence areas for sole did not yield more knowledge in this study. We implemented ICES working group values for natural mortality, weight-at-age (Table S1) and maturity-at-age43. Recruitment occurs at the beginning of each year, individuals being recruited at age 2 (ages 0–1 were not modelled; Table S4). We implemented ICES working group estimates27 for abundance at initial time step (Table S14).Norway lobsterThe stock has a sex-size structure, with 1 mixed recruitment class at 0 cm; 33 length classes for males at 2 carapace length mm intervals, from [10;12[to [72;74[carapace length mm; 23 length classes for females at 2 carapace length mm intervals, from [10;12[to [52;54[carapace length mm. A single presence area was defined: the Great Mudbank21 (see Supplementary Information’s section 2.2 and Figure S1). Several seasonal processes occur for this stock, impacting recruitment, accessibility and growth: 1/ January, begins with the annual recruitment. Females are inside their burrows, less accessible; 2/ February-March females are inside their burrows, less accessible; 3/ April: Spring moulting, females are more accessible; 4–5/ May-August females are more accessible; 6/ September, females are inside their burrows, less accessible; 7/ October: Autumn moulting only for immature females and all males, females are inside their burrows, less accessible; 8/ November-December, females are inside their burrows, less accessible44. We implemented ICES working group values for natural mortality, weight-at-class and maturity-at-class45,46,47. Growth occurs twice a year, when moulting in April and October, and is modelled with growth increments. Recruitment occurs at the beginning of each year, modelled with a Beverton-Holt relationship26, and was assumed to have the same spatial distribution as spawning stock biomass. Abundance at initial step was derived from LANGOLF survey observations and ICES WGBIE estimates25,26 (Table S16).About exploitationThe fishing exploitation structure (fleets, strategies, métiers and gears) were derived following a classification method on SACROIS 2010 landings and effort data13,23 from French fleets, and taken from a TECTAC project (https://cordis.europa.eu/project/id/Q5RS-2002-01291) database for Spanish trawlers. More details on their definition are provided in Supplementary Information’s section 2.3, Tables S5–S9 and S20–S21 and Figure S3. Spanish longliners and gillnetters fleets exploitation was described based on catch (observations from Intercatch48) rather than effort.Hake selectivity and discarding functions (one for each gear) were taken from estimates of a spatial hake stock assessment model21. Parameters values and formulæ are provided in Supplementary Information’s section 2.3 and Tables S6-S7. On top of this, inter-annual fleet dynamics factors were included in equation (21) of ISIS-Fish documentation8 in order to account for observed catch temporal variations. These factors are therefore multiplicative parameters of the target factor of each species for each métier. They are computed using observed catch27 and differ according to the period and targeted species:

    over 2010–2016, it is a ratio of observed catch in weight per year over catch observations for 2010: for hake, one per métier *season*year (left(frac{ObservedCatc{h}_{metier,season,year}}{ObservedCatc{h}_{metier,season,2010}}right)), for sole, one per métier *year (left(frac{ObservedCatc{h}_{metier,year}}{ObservedCatc{h}_{metier,2010}}right)), and for Norway lobster, one per year (identical for each métier catching Norway lobster) (left(frac{ObservedCatc{h}_{year}}{ObservedCatc{h}_{2010}}right));

    over 2017–2020: at the time of writing these assumptions, more recent data was not available, and ratios were deduced from trends on 2014–2016. A linear model was fitted on ratios deduced earlier on 2014–2016. If a significant trend was identified (hake: whitefish trawlers quarters 2 and 4, longliners and gillnetters seasons 2–3; sole and Norway lobster: all métiers), the slope was used to deduce 2017–2020 ratios (the slope was halved for hake whitefish trawlers and sole and Norway lobster values to avoid unrealistic high values of effort). Otherwise, 2016 ratios were used.

    All values are provided in Supplementary Information’s section A.2 Tables S22–S24, and the final values of target factors are derived from the Calibration procedure.About managementWe implemented a set of management rules close to what is currently implemented in the Bay of Biscay.All stocks are managed by TALs (Total Allowable Landings) until 2015 and then by TACs (Total Allowable Catch), except for Norway lobster, managed by TALs on the whole time series, not being under the landings obligation. To favour a better parametrisation, allowing for more reliable dynamics on the following years of the time series, no TALs were implemented during the calibration period (2010–2012; Fig. 1). These regulations were implemented from 2013 using historically TALs and TACs values24.Landings of the three stocks are also constrained by a Minimum Conservation Reference Size regulation that was implemented for all stocks using values currently enforced in the studied fishery28. Likewise, from 2016, the Landings Obligation was implemented, with de minimis exemptions for hake and sole, depending on the year and the gear used to fish them2,31,32,33,34. See Supplementary Information’s sections 2.4 and A.3, Figure S2 and Table S10 for further details on these restrictions.In response to the above management rules, a fishers’ behaviour algorithm has been developed to describe fishermen adaptation. Some métiers may be forbidden, depending on some conditions – the catch quota has been reached, the landings obligation is enforced – but also some values – the proportion of discarded catch, and also catch on previous years. Therefore fishermen change métiers within their strategy métiers set through a re-allocation of fishing effort to the latter set. This re-allocation aims to avoid quota overshooting. Further details about this algorithm are provided in the Supplementary Information’s sections 2.4 and A.3 and Figure S2.Calibration procedureThe model has been calibrated using two parameters (population accessibility and fishing target factor) involved in the catchability process (equation (21) in ISIS-Fish documentation8). The objective of the calibration is to reproduce the dynamics of catch over 2010–2012 at the species*métiers group scale, for each year or quarter depending on available data’s granularity. Calibration is sequentially performed: accessibility parameters for each population were estimated first followed by the target factors. The estimation of each parameter set (parameter type * population) combination was separated, and values were estimated jointly within each parameter set. To account for the specificity of each population model dynamics (global age-based for sole, spatial and size-based for hake, spatial, sex and size-based for Norway lobster), an objective function is defined for each population to calibrate their accessibility. More details on objective functions and procedures are provided in Supplementary Information’s section 2.5, as well as estimated values in Tables S17–S19.Hake accessibilityThe calibration for hake accessibility is based on a procedure developed for a former version of the database25. One parameter was estimated per quarter, all values being equal across length classes. The model outputs were fitted to hake catch observations in weight in the Bay of Biscay in 2010–2012 per length class.Sole accessibilityOne parameter was estimated per age class. The model outputs were fitted to WGBIE fishing mortality per age class for sole27 in 2010–2012.Norway lobster accessibilityOne parameter was calibrated per sex and length class. The model outputs were fitted to catch in numbers per length class and sex in 2010 per quarter provided by WGBIE.About target factorsTarget factors drive how the effort is distributed between populations, métiers and season*year combinations. They were split in 3 components: a fixed component derived from the SACROIS effort dataset analysis (Tables S25–S27), another fixed component driving inter-annual variations of fishing effort (Tables S22–S24), derived from catch observations, and finally an estimated component (Tables S28–S30), allowing to tune the model’s dynamics to observed catch. This section focuses on the estimation of the latter.Hake target factors20 parameters were defined, for each combination of the 5 groups of métiers (longliners, gillnetters, whitefish trawler (coastal), whitefish trawler (not coastal), Norway lobster trawler, see definition Table S8) and 4 quarters. We fitted the model’s outputs to the same data and with the same objective function as for hake’s accessibilities estimation.Sole target factors1 estimated component per group of métiers (gillnetters, Norway lobster trawlers and whitefish trawlers) and quarter. We fitted the model’s outputs to sole catch in weight on 2010–2012 for each métier and quarter.Norway lobster target factors1 estimated component per group of métiers (Norway lobster trawlers and whitefish trawlers). We fitted the model’s outputs to monthly Norway lobster landings data per length and sex class for 2010.Base simulationThe base simulation ran from January 2010 to December 2020 inclusive, with a monthly time step, using the database and parameters values described in this document. Several outputs of interest may be explored after a run: catch (discards and landings), as done in several figures in this paper, but also biomass (total biomass or mature biomass), fishing mortality values, or effort, all at a fine spatio-temporal scale. More

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    Genetic structure of American bullfrog populations in Brazil

    Clavero, M. & García-Berthou, E. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20(3), 5451. https://doi.org/10.1016/j.tree.2005.01.003 (2005).Article 

    Google Scholar 
    Duenas, M. A., Hemming, D. J., Roberts, A. & Diaz-Soltero, H. The threat of invasive species to IUCN-listed critically endangered species: a systematic review. Glob. Ecol. Conserv. p. e01476 (2021).Diagne, C. et al. InvaCost, a public database of the economic costs of biological invasions worldwide. Sci. Data 7(1), 1–12 (2020).Article 

    Google Scholar 
    Cuthbert, R. N. et al. Global economic costs of aquatic invasive alien species. Sci. Total Environ. 775, 145238 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Diagne, C. et al. High and rising economic costs of biological invasions worldwide. Nature 592(7855), 571–576 (2021).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Gregory, R. & Long, G. Using structured decision making to help implement a precautionary approach to endangered species management. Risk Anal. 29(4), 518–532. https://doi.org/10.1111/j.1539-6924.2008.01182.x (2009).Article 
    PubMed 

    Google Scholar 
    Berroneau, M., Detaint, M. & Coi, C. Bilan du programme de mise en place d’une stratégie d’éradication de la grenouille taureau Lithobates catesbeianus (Shaw 1802) en Aquitaine (2003–2007) et perspectives. Bull. Soc. Herpétol. France 127, 35–45 (2008).
    Google Scholar 
    Orchard, S. A. Removal of the American bullfrog, Rana (Lithobates) catesbeiana, from a pond and a lake on Vancouver Island, British Columbia, Canada. Island invasives: eradication and management. IUCN (Gland, Switzerland), 1–542 (2011).Robertson, B. C. & Gemmell, N. J. Defining eradication units to control invasive pests. J. Appl. Ecol. 41(6), 1042–1048 (2004).Article 

    Google Scholar 
    Shaw, G. General Zoology or Systematic Natural History Vol. 3, 106–108 (Society for the study of Amphibians and Reptiles, 1802).
    Google Scholar 
    Howard, R. D. Sexual dimorphism in bullfrogs. Ecology 62(2), 303–310 (1981).Article 

    Google Scholar 
    Kaefer, Í. L., Boelter, R. A. & Cechin, S. Z. Reproductive biology of the invasive bullfrog Lithobates catesbeianus in southern Brazil. In Annales Zoologici Fennici 435–444 (2007).Bissattini, A. M. & Vignoli, L. Let’s eat out, there’s crayfish for dinner: American bullfrog niche shifts inside and outside native ranges and the effect of introduced crayfish. Biol. Invasions 19(9), 2633–2646 (2017).Article 

    Google Scholar 
    Boelter, R. A. & Cechin, S. Z. Impacto da dieta de rã-touro (Lithobates catesbeianus – Anura, Ranidae) sobre a fauna nativa: estudo de caso na região de Agudo – RS – Brasil 1. Nat. Conserv. 5(2), 45–53 (2007).
    Google Scholar 
    Govindarajulu, P., Price, W. S. & Anholt, B. R. Introduced bullfrogs (Rana catesbeiana) in western Canada: has their ecology diverged?. J. Herpetol. 40(2), 249–261 (2006).Article 

    Google Scholar 
    McCoy, C. J. Diet of bullfrogs (Rana catesbeiana) in Central Oklahoma farm ponds. In Proceedings of the Oklahoma Academy of Sciences 44–45 (1967).Teixeira, E., Silva, D., Pinto, O., Filho, R. & Feio, R. N. Predation of native anurans by invasive bullfrogs in Southeastern Brazil: spatial variation and effect of microhabitat use by prey. S. Am. J. Herpetol. 6(1), 1–11. https://doi.org/10.2994/057.006.0101 (2011).Article 

    Google Scholar 
    Wu, Z., Li, Y., Wang, Y. & Adams, M. J. Diet of introduced Bullfrogs (Rana catesbeiana): predation on and diet overlap with native frogs on Daishan Island China. J. Herpetol. 39(4), 668–675 (2005).Article 

    Google Scholar 
    Howard, R. D. The influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecol. Soc. Am. 59(4), 789–798 (1978).
    Google Scholar 
    Van Wilgen, N. J., Gillespie, M. S., Richardson, D. M. & Measey, J. A taxonomically and geographically constrained information base limits non-native reptile and amphibian risk assessment: a systematic review. PeerJ 6, 5850 (2018).Article 

    Google Scholar 
    Sales, L., Rebouças, R. & Toledo, L. F. Native range climate is insufficient to predict anuran invasive potential. Biol. Invasions 23, 2635–2647 (2021).Article 

    Google Scholar 
    Kumschick, S. et al. How repeatable is the Environmental Impact Classification of Alien Taxa (EICAT)? Comparing independent global impact assessments of amphibians. Ecol. Evol. 7(8), 2661–2670 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kupferberg, S. J. Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78(6), 1736–1751 (1997).Article 

    Google Scholar 
    Toledo, L. F., Ribeiro, R. S. & Haddad, C. F. Anurans as prey: an exploratory analysis and size relationships between predators and their prey. J. Zool. 271(2), 170–177 (2007).Article 

    Google Scholar 
    Daszak, P. et al. Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol. J. 14, 201–208 (2004).
    Google Scholar 
    Gervasi, S. S. et al. Experimental evidence for American bullfrog (Lithobates catesbeianus) susceptibility to chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 10(2), 166–171 (2013).PubMed 
    Article 

    Google Scholar 
    Urbina, J., Bredeweg, E. M., Garcia, T. S. & Blaustein, A. R. Host–pathogen dynamics among the invasive American bullfrog (Lithobates catesbeianus) and chytrid fungus (Batrachochytrium dendrobatidis). Hydrobiologia 817(1), 267–277 (2018).CAS 
    Article 

    Google Scholar 
    Schloegel, L. M. et al. The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Anim. Conserv. 13, 53–61. https://doi.org/10.1111/j.1469-1795.2009.00307.x (2010).Article 

    Google Scholar 
    Ohanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360(6389), 621–627 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Adams, A. J. et al. Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian. Ecosphere 8(3), 01740 (2017).Article 

    Google Scholar 
    Santos, R. C. et al. High prevalence and low intensity of infection by Batrachochytrium dendrobatidis in rainforest bullfrog populations in southern Brazil. Herpetol. Conserv. Biol. 15(1), 118–130 (2020).
    Google Scholar 
    Ribeiro, L. P. et al. Bullfrog farms release virulent zoospores of the frog-killing fungus into the natural environment. Sci. Rep. 9, 13422 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Both, C. & Grant, T. Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biol. Let. 8(5), 1–3. https://doi.org/10.1098/rsbl.2012.0412 (2012).Article 

    Google Scholar 
    Medeiros, C. I., Both, C., Grant, T. & Hartz, S. M. Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls. Biol. Invasions 19(2), 675–690 (2017).Article 

    Google Scholar 
    Ferrante, L., Kaefer, I. L. & Baccaro, F. B. Aliens in the backyard: Did the American bullfrog conquer the habitat of native frogs in the semi-deciduous Atlantic Forest?. Herpetol. J. 30, 93–98 (2020).Article 

    Google Scholar 
    da Silva Silveira, S. & Guimarães, M. The enemy within: consequences of the invasive bullfrog on native anuran populations. Biol. Invasions 23(2), 373–378 (2021).Article 

    Google Scholar 
    Kraus, F. Impacts from invasive reptiles and amphibians. Annu. Rev. Ecol. Evol. Syst. 46, 75–97 (2015).Article 

    Google Scholar 
    Ribeiro, L. P. & Toledo, L. F. An overview of the Brazilian frog farming. Aquaculture 548, 737623 (2022).Article 

    Google Scholar 
    Cunha, E. R. & Delariva, R. L. Introdução da rã-touro, Lithobates catesbeianus (SHAW, 1802): uma revisão. Saúde e Biologia 4(2), 34–46 (2009).
    Google Scholar 
    Ferreira, C. M., Pimenta, A. G. C. & Neto, J. S. P. Introdução à ranicultura. Boletim Técnico Do Instituto de Pesca 33, 15 (2002).
    Google Scholar 
    Fontanello, D. & Ferreira, C. M. Histórico da ranicultura nacional. Instituto de Pesca de São Paulo (2007).Both, C. et al. Widespread occurrence of the American bullfrog, Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae), in Brazil. S. Am. J. Herpetol. 6(2), 127–135 (2011).Article 

    Google Scholar 
    Bai, C., Ke, Z., Consuegra, S., Liu, X. & Yiming, L. The role of founder effects on the genetic structure of the invasive bullfrog (Lithobates catesbeianaus) in China. Biol. Invasions 14, 1785–1796. https://doi.org/10.1007/s10530-012-0189-x (2012).Article 

    Google Scholar 
    Liu, X. & Li, Y. Aquaculture enclosures relate to the establishment of feral populations of introduced species. PLoS ONE https://doi.org/10.1371/journal.pone.0006199 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Santos-pereira, M. & Rocha, C. F. D. Invasive bullfrog Lithobates catesbeianus (Anura: Ranidae) in the Paraná state, Southern Brazil : a summary of the species spread. Revista Brasileira De Zoociências 16, 141–147 (2015).
    Google Scholar 
    Moreira, C. R., Henriques, M. B. & Ferreira, C. M. Frog farms as proposed in agribusiness aquaculture: economic viability based in feed conversion. Pesca Inst. Bull. 39(4), 389–399 (2018).
    Google Scholar 
    Ficetola, G. F., Thuiller, W. & Miaud, C. Prediction and validation of the potential global distribution of a problematic alien invasive species – The American bullfrog. Divers. Distrib. 13(4), 476–485. https://doi.org/10.1111/j.1472-4642.2007.00377.x (2007).Article 

    Google Scholar 
    Funk, W. C., Garcia, T. S., Cortina, G. A. & Hill, R. H. Population genetics of introduced bullfrogs, Rana (Lithobates) catesbeianus, in the Willamette Valley, Oregon, USA. Biol. Invasions 13, 651–658. https://doi.org/10.1007/s10530-010-9855-z (2011).Article 

    Google Scholar 
    Rollins, L. A., Woolnough, A. P., Wilton, A. N., Sinclair, R. & Sherwin, W. B. Invasive species can’t cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol. Ecol. 18, 1560–1573. https://doi.org/10.1111/j.1365-294X.2009.04132.x (2009).Article 
    PubMed 

    Google Scholar 
    Schwartz, M. K., Luikart, G. & Waples, R. S. Genetic monitoring as a promising tool for conservation and management. Trends Ecol. Evol. 22(1), 25–33. https://doi.org/10.1016/j.tree.2006.08.009 (2007).Article 
    PubMed 

    Google Scholar 
    Ficetola, G. F., Bonin, A. & Miaud, C. Population genetics reveals origin and number of founders in a biological invasion. Mol. Ecol. 17, 773–782. https://doi.org/10.1111/j.1365-294X.2007.03622.x (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kamath, P. L., Sepulveda, A. J. & Layhee, M. Genetic reconstruction of a bullfrog invasion to elucidate vectors of introduction and secondary spread. Ecol. Evol. 6(15), 5221–5233. https://doi.org/10.1002/ece3.2278 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Du Sert, N. P. et al. Reporting animal research: explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol. 18(7), e3000411 (2020).Article 
    CAS 

    Google Scholar 
    Austin, J. D. Genetic evidence for female-biased dispersal in the bullfrog, Rana catesbeiana (Ranidae). Mol. Ecol. 12(11), 3165–3172. https://doi.org/10.1046/j.1365-294X.2003.01948.x (2003).Article 
    PubMed 

    Google Scholar 
    Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M. & Shipley, P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4(3), 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x (2004).CAS 
    Article 

    Google Scholar 
    Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11(1), 94. https://doi.org/10.1186/1471-2156-11-94 (2010).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jombart, T. Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24(11), 1403–1405. https://doi.org/10.1093/bioinformatics/btn129 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    Jost, L. GST and its relatives do not measure differentiation. Mol. Ecol. 17(18), 4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x (2008).Article 
    PubMed 

    Google Scholar 
    Winter, D. J. MMOD: An R library for the calculation of population differentiation statistics. Mol. Ecol. Resour. 12(6), 1158–1160. https://doi.org/10.1111/j.1755-0998.2012.03174.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gerlach, G. Calculations of population differentiation based on GST and D: forget GST but not all of statistics!. Mol. Ecol. 19(18), 3845–3852 (2010).PubMed 
    Article 

    Google Scholar 
    Hochberg, Y. & Benjamini, Y. More powerful procedures for multiple statistical significance testing. Stat. Med. 9, 811–818 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hauser, S., Wakeland, K. & Leberg, P. Inconsistent use of multiple comparison corrections in studies of population genetic structure: Are some type I errors more tolerable than others?. Mol. Ecol. Resour. 19(1), 144–148 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Team R Core. R: A language and environment for statistical computing. R Foundation for Statistical Computing URL. Vienna, Austria. Retrieved from https://www.r-project.org/. (2017).Dyer, R. J. gstudio: Analyses and functions related to the spatial analysis of genetic marker data. R Package Version (2014).Rousset, F. GENEPOP’007: A complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 8(1), 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x (2008).Article 
    PubMed 

    Google Scholar 
    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155(2), 945–959 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Earl, D. A., vonHoldt, B. & M.,. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4(2), 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).Article 

    Google Scholar 
    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10(3), 564–567 (2010).PubMed 
    Article 

    Google Scholar 
    Moritz, C., Schneider, C. J. & Wake, D. B. Evolutionary relationships within the Ensatina eschscholtzii complex confirm the ring species interpretation. Syst. Biol. 41(3), 273–291 (1992).Article 

    Google Scholar 
    Goebel, A. M., Donnelly, J. M. & Atz, M. E. PCR primers and amplification methods for 12S ribosomal DNA, the control region, cytochrome oxidase I, and cytochromebin bufonids and other frogs, and an overview of PCR primers which have amplified DNA in amphibians successfully. Mol. Phylogenet. Evol. 11(1), 163–199 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kearse, M. et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 1647–1649 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30(4), 772–780 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Labonne, J. et al. From the bare minimum: genetics and selection in populations founded by only a few parents. Evol. Ecol. Res. 17(1), 21–34 (2016).
    Google Scholar 
    Chapuis, M. P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24(3), 621–631 (2006).PubMed 
    Article 
    CAS 

    Google Scholar 
    Carlsson, J. Effects of microsatellite null alleles on assignment testing. J. Hered. 99(6), 616–623 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Consuegra, S., Phillips, N., Gajardo, G. & Leaniz, C. G. Winning the invasion roulette: escapes from fish farms increase admixture and facilitate establishment of non-native rainbow trout. Evol. Appl. 4, 660–671. https://doi.org/10.1111/j.1752-4571.2011.00189.x (2011).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Peacock, M. M., Beard, K. H., O’Neill, E. M., Kirchoff, V. S. & Peters, M. B. Strong founder effects and low genetic diversity in introduced populations of Coqui frogs. Mol. Ecol. 18(17), 3603–3615. https://doi.org/10.1111/j.1365-294X.2009.04308.x (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Austin, J. D., Lougheed, S. C. & Boag, P. T. Discordant temporal and geographic patterns in maternal lineages of eastern north American frogs, Rana catesbeiana (Ranidae) and Pseudacris crucifer (Hylidae). Mol. Phylogenet. Evol. 32, 799–816. https://doi.org/10.1016/j.ympev.2004.03.006 (2004).Article 
    PubMed 

    Google Scholar 
    Selechnik, D. et al. Increased adaptive variation despite reduced overall genetic diversity in a rapidly adapting invader. Front. Genet. 10, 1221 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Predicting ecological impacts of the invasive brush-clawed shore crab under environmental change

    Simberloff, D. et al. Impacts of biological invasions: What’s what and the way forward. Trends Ecol. Evol. 28, 58–66 (2013).PubMed 
    Article 

    Google Scholar 
    Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. 95(6), 1511–1534 (2020).PubMed 
    Article 

    Google Scholar 
    Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bailey, S. A. et al. Trends in the detection of aquatic non–indigenous species across global marine, estuarine and freshwater ecosystems: A 50–year perspective. Divers. Distrib. 26, 1780–1797 (2020).MathSciNet 
    Article 

    Google Scholar 
    Ricciardi, A. Are modern biological invasions an unprecedented form of global change?. Conserv. Biol. 21, 329–336 (2007).PubMed 
    Article 

    Google Scholar 
    Meyerson, M. Invasive alien species in an era of globalization. Front. Ecol. Environ. 5, 199–208 (2007).Article 

    Google Scholar 
    Hulme, P. E. Trade, transport and trouble: Managing invasive species pathways in an era of globalization. J. Appl. Ecol. 46, 10–18 (2009).Article 

    Google Scholar 
    Bonnamour, A., Gippet, J. M. & Bertelsmeier, C. Insect and plant invasions follow two waves of globalisation. Ecol. Lett. 24(11), 2418–2426 (2021).PubMed 
    Article 

    Google Scholar 
    Piola, R. F. & Johnston, E. L. Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Divers. Distrib. 14, 329–342 (2008).Article 

    Google Scholar 
    Rahel, F. J. & Olden, J. D. Assessing the effects of climate change on aquatic invasive species. Conserv. Biol. 22, 521–533 (2008).PubMed 
    Article 

    Google Scholar 
    Kenworthy, J. M., Davoult, D. & Lejeusne, C. Compared stress tolerance to short-term exposure in native and invasive tunicates from the NE Atlantic: When the invader performs better. Mar. Biol. 165(10), 1–11 (2018).Article 

    Google Scholar 
    Gollasch, S., Galil, B. S., & Cohen, A. N. Bridging divides: Maritime canals as invasion corridors. In Bridging Divides: Maritime Canals as Invasion Corridors (Vol. 83). https://doi.org/10.1007/978-1-4020-5047-3 (2006).Galil, B. S. et al. ‘Double trouble’: The expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biol. Invasions 17, 973–976 (2015).Article 

    Google Scholar 
    Jeschke, J. et al. Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14, 1–20 (2012).Article 

    Google Scholar 
    Lowry, E. et al. Biological invasions: A field synopsis, systematic review, and database of the literature. Ecol. Evol. 3, 182–196 (2012).PubMed 
    Article 

    Google Scholar 
    Brockerhoff, A., & McLay, C. Human-Mediated Spread of Alien Crabs. In In the Wrong Place – Alien Marine Crustaceans: Distribution, Biology and Impacts (pp. 27–106). Springer Netherlands. https://doi.org/10.1007/978-94-007-0591-3_2 (2011).Hammock, B. G. et al. Low food availability narrows the tolerance of the copepod eurytemora affinis to salinity, but not to temperature. Estuar. Coasts 39, 189–200 (2016).CAS 
    Article 

    Google Scholar 
    Rato, L. D., Crespo, D. & Lemos, M. F. L. Mechanisms of bioinvasions by coastal crabs using integrative approaches – A conceptual review. Ecol. Ind. 125, 107578 (2021).Article 

    Google Scholar 
    Weis, J. S. The role of behavior in the success of invasive crustaceans. Mar. Freshw. Behav. Physiol. 43, 83–98 (2010).Article 

    Google Scholar 
    Hänfling, B., Edwards, F. & Gherardi, F. Invasive alien Crustacea: Dispersal, establishment, impact and control. Biocontrol 56, 573–595 (2011).Article 

    Google Scholar 
    Kouba, A. et al. Identifying economic costs and knowledge gaps of invasive aquatic crustaceans. Sci. Total Environ. 813, 152325 (2022).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Geburzi, J. C., & McCarthy, M. L. How Do They Do It? – Understanding the Success of Marine Invasive Species. In YOUMARES 8 – Oceans Across Boundaries: Learning from each other (pp. 109–124). Springer International Publishing. https://doi.org/10.1007/978-3-319-93284-2_8 (2018).Casties, I. & Briski, E. Life history traits of aquatic non-indigenous species: Freshwater vs. marine habitats. Aquat. Invasions 14, 566–581 (2019).Article 

    Google Scholar 
    Grosholz, E. D. & Ruiz, G. M. Predicting the impact of introduced marine species: Lessons from the multiple invasions of the European green crab Carcinus maenas. Biol. Cons. 78, 59–66 (1996).Article 

    Google Scholar 
    Geburzi, J., Graumann, G., Köhnk, S. & Brandis, D. First record of the Asian crab Hemigrapsus takanoi Asakura & Watanabe, 2005 (Decapoda, Brachyura, Varunidae) in the Baltic Sea. BioInvasions Rec. 4, 103–107 (2015).Article 

    Google Scholar 
    Briski, E., Ghabooli, S., Bailey, S. A. & MacIsaac, H. J. Invasion risk posed by macroinvertebrates transported in ships’ ballast tanks. Biol. Invasions 14, 1843–1850 (2012).Article 

    Google Scholar 
    Wasserstraßen-und Schifffahrtsverwaltung des Bundes. Halbjahresbilanz Nord-Ostsee-Kanal 2021. www.wsv.de (2021).Nour, O. M., Stumpp, M., Morón Lugo, S. C., Barboza, F. R. & Pansch, C. Population structure of the recent invader Hemigrapsus takanoi and prey size selection on Baltic Sea mussels. Aquat. Invasions 15, 297–317 (2020).Article 

    Google Scholar 
    Andersson, A. et al. Projected future climate change and Baltic Sea ecosystem management. Ambio 44(Suppl 3), 345–356 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    BACC Author Team. Assessment of Climate Change for the Baltic Sea Basin. (2008).BACC Author Team. Second Assessment of Climate Change for the Baltic Sea Basin. (2015).Meier, H. E. M. et al. Modeling the combined impact of changing climate and changing nutrient loads on the Baltic Sea environment in an ensemble of transient simulations for 1961–2099. Clim. Dyn. 39, 2421–2441 (2012).Article 

    Google Scholar 
    Meier, H. E. M. et al. Climate change in the baltic sea region: A summary. Earth Syst. Dyn. Discuss. https://doi.org/10.5194/esd-2021-67 (2021).Article 

    Google Scholar 
    Ricciardi, A. et al. Four priority areas to advance invasion science in the face of rapid environmental change. Environ. Rev. 29, 119–141 (2021).Article 

    Google Scholar 
    Solomon, M. E. The natural control of animal populations. J. Anim. Ecol. 18, 1–35 (1949).Article 

    Google Scholar 
    Holling, C. S. Some characteristics of simple types of predation and parasitism. Can. Entomol. 91, 385–398 (1959).Article 

    Google Scholar 
    Dick, J. T. A. et al. Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biol. Invasions 16, 735–753 (2014).Article 

    Google Scholar 
    Laverty, C. et al. Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biol. Invasions 19, 1653–1665 (2017).Article 

    Google Scholar 
    Anton, A. et al. Global ecological impacts of marine exotic species. Nat. Ecol. Evol. 3, 787–800 (2019).PubMed 
    Article 

    Google Scholar 
    Crystal-Ornelas, R. & Lockwood, J. L. The ‘known unknowns’ of invasive species impact measurement. Biol. Invasions 22, 1513–1525 (2020).Article 

    Google Scholar 
    Boudreau, S. A. & Worm, B. Ecological role of large benthic decapods in marine ecosystems: A review. Mar. Ecol. Prog. Ser. 469, 195–213 (2012).ADS 
    Article 

    Google Scholar 
    Dick, J. T. A. et al. Invader relative impact potential: A new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. J. Appl. Ecol. 54, 1259–1267 (2017).Article 

    Google Scholar 
    Cornelius, A., Wagner, K. & Buschbaum, C. Prey preferences, consumption rates and predation effects of Asian shore crabs (Hemigrapsus takanoi) in comparison to native shore crabs (Carcinus maenas) in northwestern Europe. Mar. Biodivers. 51(5), 1–17 (2021).Article 

    Google Scholar 
    Elner, R. W. The influence of temperature, sex and chela size in the foraging strategy of the shore crab, Carcinus maenas (L.). Mar. Behav. Physiol. 7, 15–24 (1980).Article 

    Google Scholar 
    Brose, U. Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct. Ecol. 24, 28–34 (2010).Article 

    Google Scholar 
    Cuthbert, R. N. et al. Influence of intra- and interspecific variation in predator-prey body size ratios on trophic interaction strengths. Ecol. Evol. 10, 5946–5962 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Payne, A. & Kraemer, G. P. Morphometry and claw strength of the non-native asian shore crab, Hemigrapsus sanguineus. Northeast. Nat. 20, 478–492 (2013).Article 

    Google Scholar 
    Sedova, L. G. The effect of temperature on the rate of oxygen consumption in the sea urchin Strongylocentrotus intermedius. Russ. J. Mar. Biol. 26, 51–53 (2000).Article 

    Google Scholar 
    Saucedo, P. E., Ocampo, L., Monteforte, M. & Bervera, H. Effect of temperature on oxygen consumption and ammonia excretion in the Calafa mother-of-pearl oyster, Pinctada mazatlanica (Hanley, 1856). Aquaculture 229, 377–387 (2004).Article 

    Google Scholar 
    Nie, H. et al. Effects of temperature and salinity on oxygen consumption and ammonia excretion in different colour strains of the Manila clam, Ruditapes philippinarum. Aquac. Res. 48, 2778–2786 (2017).CAS 
    Article 

    Google Scholar 
    Nguyen, K. D. T. et al. Upper Temperature limits of tropical marine ectotherms: Global warming implications. PLoS ONE 6, e29340 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tattersall, G. J. et al. Coping with thermal challenges: Physiological adaptations to environmental temperatures. In Comprehensive Physiology 2151–2202 (Wiley, Hoboken, 2012).Chapter 

    Google Scholar 
    Barrios-O’Neill, D., Dick, J. T., Emmerson, M. C., Ricciardi, A. & MacIsaac, H. J. Predator-free space, functional responses and biological invasions. Funct. Ecol. 29(3), 377–384 (2015).Article 

    Google Scholar 
    Tattersall, G. J. et al. Coping with Thermal Challenges: Physiological Adaptations to Environmental Temperatures Vol. 2 (Wiley, Hoboken, 2012).
    Google Scholar 
    Bollache, L., Dick, J., Farnsworth, K. & Montgomery, I. Comparison of the functional responses of invasive and native amphipods. Biol. Lett. 4, 166–169 (2008).PubMed 
    Article 

    Google Scholar 
    Dick, J. T. A. et al. Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol. Invasions 15, 837–846 (2013).Article 

    Google Scholar 
    Cuthbert, R. N., Dickey, J. W. E., Coughlan, N. E., Joyce, P. W. S. & Dick, J. T. A. The functional response ratio (FRR): Advancing comparative metrics for predicting the ecological impacts of invasive alien species. Biol. Invasions 21, 2543–2547 (2019).Article 

    Google Scholar 
    Englund, G., Ohlund, G., Hein, C. L. & Diehl, S. Temperature dependence of the functional response. Ecol Lett 14, 914–921 (2011).PubMed 
    Article 

    Google Scholar 
    Jeschke, J. M., Kopp, M. & Tollrian, R. Predator functional responses: Discriminating between handling and digesting prey. Ecol. Monogr. 72(1), 95–112 (2002).Article 

    Google Scholar 
    Dell, A. I., Pawar, S. & van Savage, M. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl. Acad. Sci. U.S.A 108, 10591–10596 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    South, J., Welsh, D., Anton, A., Sigwart, J. D. & Dick, J. T. A. Increasing temperature decreases the predatory effect of the intertidal shanny Lipophrys pholis on an amphipod prey. J. Fish Biol. 92, 150–164 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Pörtner, H.-O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Dickey, J. W. E. et al. Breathing space: Deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages. Biol. Invasions 23, 2831–2847 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Watanabe, S., Wilder, M. N., Strüssmann, C. A. & Shinji, J. Short-term responses of the adults of the common Japanese intertidal crab, Hemigrapsus takanoi (Decapoda: Brachyura: Grapsoidea) at different salinities: Osmoregulation, oxygen consumption, and ammonia excretion. J. Crustac. Biol. 29, 269–272 (2009).Article 

    Google Scholar 
    Wasserman, R. J. et al. Using functional responses to quantify interaction effects among predators. Funct. Ecol. 30, 1988–1998 (2016).Article 

    Google Scholar 
    Murdoch, W. W. Switching in general predators: Experiments on predator specificity and stability of prey populations. Ecol. Monogr. 39, 335–354 (1969).Article 

    Google Scholar 
    Gonzalez, A., Lambert, A. & Ricciardi, A. When does ecosystem engineering cause invasion and species replacement?. Oikos 117, 1247–1257 (2008).Article 

    Google Scholar 
    King, J. R. & Tschinkel, W. R. Experimental evidence that human impacts drive fire ant invasions and ecological change. Proc. Natl. Acad. Sci. U.S.A 105, 20339–20343 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Asakura, A. & Watanabe, S. Hemigrapsus takanoi, new species, a sibling species of the common Japanese Intertidal Crab H. penicillatus (Decapoda: Brachyura: Grapsoidea). J. Crustac. Biol. 25, 279–292 (2005).Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (2021).Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.4.3, https://CRAN.R-project.org/package=DHARMa (2021).Crawley, M. J. The R Book (Wiley, Hoboken, 2007).MATH 
    Book 

    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, Thousand Oaks, 2019).
    Google Scholar 
    Lenth, R. v. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.6.2-1, https://CRAN.R-project.org/package=emmeans (2021).Pritchard, D. frair: Tools for Functional Response Analysis. R package version 0.5.100, https://CRAN.R-project.org/package=frair (2017).Juliano, S.A., Nonlinear Curve Fitting: Predation and Functional Response Curves. In: Cheiner, S.M. and Gurven, J., Eds., Design and Analysis of Ecological Experiments, 2nd Edition, Chapman and Hall, London, 178–196. (2001)Rogers, D. Random search and insect population models. J. Anim. Ecol. 41, 369 (1972).Article 

    Google Scholar  More

  • in

    Plant tissue characteristics of Miscanthus x giganteus

    Geospatial dataSampling locations were established, flagged, and recorded in June 2016, using a Trimble Geo7X global navigation satellite system (GNSS) receiver using the Trimble® VRS Now real-time kinematic (RTK) correction. Location accuracies were verified to within ±2 cm. Points were imported into a geodatabase using Esri ArcMap (Advanced license, Version 10.5) and projected using the Universal Transverse Mercator (UTM), Zone 17 North projection, with the 1983 North American datum (NAD83). Field investigators navigated to the flagged locations by visually locating them in the field or by using recreational grade GNSS receivers with the locations stored as waypoints.Plant tissue sampling and preparationMiscanthus x giganteus grows in clumps of bamboo-like canes. A single cane was cut at soil level from each of the five sample collection points in each circular plot, individually labelled, and brought to the lab for processing (Fig. 2). Each stem was measured from the cut at the base to the last leaf node, and the length was recorded. Green, fully expanded leaves were cut from each stem and leaves and stems from each plant were placed in separate paper bags and dried at 60 °C. The dry leaf and stem tissues were ground to pass a 1 mm screen (Wiley Mill Model 4, Thomas Scientific, Swedesboro, New Jersey, USA). Subsamples of the ground material were analyzed for total carbon (C) and nitrogen (N), acid-digested for the analysis of total macro- and micronutrients, and water-extracted for spectroscopic analysis and the characterization of the water extractable organic matter (WEOM) (Fig. 2).Fig. 2Images of field samples, and diagram of plant tissue processing. Center panel – flow chart outlining the procedures for plant tissue processing, the kinds of analyses performed, and the type of data generated. Upper left inset panel – ground level picture of Miscanthus x giganteus circular plots. Upper right inset panel – some plant samples on the day of collection.Full size imageTotal carbon and nitrogenDried and ground leaf and stem material (~4–6 mg) was analyzed for total C and N content by combustion (Vario EL III, Elementar Americas Inc., Mt. Laurel, New Jersey, USA). The instrument was calibrated using an aspartic acid standard (36.08% C ± 0.52% and 10.53% N ± 0.18%). Validation by inclusion of two aspartic acid samples as checks in each autosampler carousel (80 wells) resulted in a net positive bias of 1.44 and 1.68% for C and N, respectively. The mean C and N concentrations and standard deviations for the sample set are presented in Table 1.Table 1 Giant miscanthus composition including leaf (L) and stem (S) dry weight, length, and carbon (C) and nitrogen (N) concentrations (n = 165). Values are reported as means ± standard deviations.Full size tableMacro- and micronutrientsPlant tissue samples were analyzed for a suite of macro- and micronutrients including aluminum (Al), arsenic (As), boron (B), calcium (Ca), cadmium (Cd), cobalt (Co), chromium (Cr), copper (Cu), iron (Fe), potassium (K), magnesium (Mg), manganese (Mn), molybdenum (Mo), sodium (Na), nickel (Ni), phosphorus (P), lead (Pb), sulfur (S), selenium (Se), silicon (Si), titanium (Ti), vanadium (V), and zinc (Zn) using Inductively Coupled Plasma with Optical Emission Spectroscopy (ICP-OES). Samples (0.5 g) were digested using 10 mL of trace metal grade nitric acid (HNO3) in a microwave digestion system (Mars 6, CEM, Matthews, North Carolina, USA). During the digestion procedure (CEM Mars 6 Plant Material Method), the oven temperature was increased from room temperature to 200 °C in 15 minutes and held at 200 °C for 10 minutes. The pressure limit of the digestion vessels was set to 800 psi although it was not monitored during individual runs. Sample digestates were transferred quantitatively to centrifuge tubes, diluted to 50 mL with 2% HNO3 (prepared with lab grade deionized water), and centrifuged at 2500 rpm for 10 min (Sorvall ST8 centrifuge, Thermo Fisher Scientific, San Jose, California, USA). The digestates were decanted into clean centrifuge tubes and analyzed using an iCAP 7400 ICP-OES Duo equipped with a Charge Injection Device detector (Thermo Fisher Scientific, San Jose, California, USA). An aliquot of digested sample was aspirated from the centrifuge tube using a CETAC ASX-520 autosampler (Teledyne CETAC Technologies, Omaha, Nebraska, USA) and passed through a concentric tube nebulizer. The resulting aerosol was then swept through the plasma using argon as the carrier gas with a flow rate of 0.5 L/min and a nebulizer gas flow rate of 0.7 L/min. Macro- and micronutrients were quantified by monitoring the emission wavelengths (Em λ) reported in Table 2.Table 2 Macro- and micronutrients measured, and emission wavelengths (Em λ) used to quantify them in the miscanthus leaves (L) and stems (S), the total number and percentage detected (n = 150 for leaves and 162 for stems), the mean detected concentration ± standard deviation, and the mean method detection limit (MDL) ± standard deviation.Full size tableCharacterization of the water extractable organic matter (WEOM)The WEOM of the giant miscanthus leaves and stems was isolated by extracting the plant material with deionized water at room temperature6. The water extractions were performed by mixing ~0.2 g of dry, ground leaves and stems with 100 mL of deionized water in 125 mL pre-washed brown Nalgene bottles. All brown Nalgene bottles used for these extractions were pre-washed by soaking them for 24 hours in a 10% hydrochloric acid solution followed by 24 hours in a 10% sodium hydroxide solution, and a thorough rinse with deionized water. The bottles containing the extraction solution were shaken on an orbital shaker at 180 rpm for 24 hours. The extract was vacuum filtered using 0.45 µm glass fibre filters (GF/F, Whatman) into pre-washed 60 mL brown Nalgene bottles. The filtered water extracts containing the WEOM were stored in the dark in a refrigerator (4 °C) until analysis by UV-Visible and fluorescence spectroscopy. Samples were visually inspected just prior to analysis to ensure no colloids or precipitates had formed during storage. Samples that had become visually cloudy were re-filtered.On the day of analysis, the water extracts were removed from the refrigerator and allowed to warm up to room temperature. Chemical characteristics of the WEOM were assessed through the analysis of optical properties on an Aqualog spectrofluorometer (Horiba Scientific, New Jersey, USA) equipped with a 150 W continuous output Xenon arc lamp. Excitation-emission matrix (EEM) scans were acquired in a 1 cm quartz cuvette with excitation wavelengths (Ex λ) scanned using a double-grating monochrometer from 240 to 621 nm at 3 nm intervals. Emission wavelengths (Em λ) were scanned from 246 to 693 nm at 2 nm intervals and emission spectra were collected using a Charge Coupled Device (CCD) detector. All fluorescence spectra were acquired in sample over reference ratio mode to account for potential fluctuations and wavelength dependency of the excitation lamp output. Samples were corrected for the inner filter effect7 and each sample EEM underwent spectral subtraction with a deionized water blank to remove the effects due to Raman scattering. Rayleigh masking was applied to remove the signal intensities for both the first and second order Rayleigh lines. Instrument bias related to wavelength-dependent efficiencies of the specific instrument’s optical components (gratings, mirrors, etc.) was automatically corrected by the Aqualog software after each spectral acquisition. The fluorescence intensities were normalized to the area under the water Raman peak collected on each day of analysis and are expressed in Raman-normalized intensity units (RU). All sample EEM processing was performed with the Aqualog software (version 4.0.0.86).The optical data obtained from the EEM scans were used to calculate several indices representative of WEOM chemical composition (Table 3) including the absorbance at 254 nm (Abs254), the ratio of the absorbance at 254 to 365 nm (Abs254:365), the ratio of the absorbance at 280 to 465 nm (Abs280:465), the spectral slope ratio (SR), the fluorescence index (FI), the humification index (HIX), the biological index (BIX), and the freshness index (β:α). The SR was calculated as the ratio of two spectral slope regions of the absorbance spectra (275–295 and 350–400 nm)8. The FI was calculated as the ratio of the emission intensities at Em λ 470 and 520 nm, at an Ex λ of 370 nm9. The HIX was calculated by dividing the emission intensity in the 435–480 nm region by the sum of emission intensities in the 300–345 and 435–480 nm regions, at an Ex λ of 255 nm10. The BIX was calculated as the ratio of emission intensities at 380 and 430 nm, at an Ex λ of 310 nm11. The freshness index β:α was calculated as the emission intensity at 380 nm divided by the maximum emission intensity between 420 and 432 nm, at an Ex λ of 310 nm12. To further characterize the giant miscanthus WEOM, the fluorescence intensity at specific excitation-emission pairs was also identified. The fluorescence peaks identified here have previously been reported for surface water samples and water extracts13 and include peak A (Ex λ 260, Em λ 450), peak C (Ex λ 340, Em λ 440), peak M (Ex λ 300, Em λ 390), peak B (Ex λ 275, Em λ 310), and peak T (Ex λ 275, Em λ 340). A brief description of these optical indices is provided in Table 3.Table 3 Description of the optical indices calculated from the excitation-emission matrix (EEM) fluorescence scans and used to analyze the WEOM composition of giant miscanthus leaves and stems.Full size table More

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    Utilisation of Oxford Nanopore sequencing to generate six complete gastropod mitochondrial genomes as part of a biodiversity curriculum

    Rasmussen, R. S. & Morrissey, M. T. Application of DNA-based methods to identify fish and seafood substitution on the commercial market. Compr. Rev. Food Sci. Food Saf. 8, 118–154 (2009).CAS 
    Article 

    Google Scholar 
    Chiu, M.-C., Huang, C.-G., Wu, W.-J. & Shiao, S.-F. A new horsehair worm, Chordodes formosanus sp. N. (Nematomorpha, Gordiida) from Hierodula mantids of Taiwan and Japan with redescription of a closely related species, Chordodes japonensis. ZooKeys 160, 1–22 (2011).Article 

    Google Scholar 
    Robins, J. H. et al. Phylogenetic species identification in Rattus highlights rapid radiation and morphological similarity of new Guinean species. PLoS One 9, e98002. https://doi.org/10.1371/journal.pone.0098002 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sutherland, W. J., Roy, D. B. & Amano, T. An agenda for the future of biological recording for ecological monitoring and citizen science. Biol. J. Linn. Soc. 115, 779–784 (2015).Article 

    Google Scholar 
    Ho, J. K. I., Puniamoorthy, J., Srivathsan, A. & Meier, R. MinION sequencing of seafood in Singapore reveals creatively labelled flatfishes, confused roe, pig DNA in squid balls, and phantom crustaceans. Food Control 112, 107144. https://doi.org/10.1016/j.foodcont.2020.107144 (2020).CAS 
    Article 

    Google Scholar 
    Elson, J. & Lightowlers, R. Mitochondrial DNA clonality in the dock: Can surveillance swing the case?. Trends Genet. 22, 603–607 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bernt, M., Braband, A., Schierwater, B. & Stadler, P. F. Genetic aspects of mitochondrial genome evolution. Mol. Phylogenet. Evol. 69, 328–338 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Blaxter, M. L. The promise of a DNA taxonomy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 669–679 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Waugh, J. DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29, 188–197 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Grandjean, F. et al. Rapid recovery of nuclear and mitochondrial genes by genome skimming from Northern Hemisphere freshwater crayfish. Zool. Scr. 46, 718–728 (2017).Article 

    Google Scholar 
    Trevisan, B., Alcantara, D. M. C., Machado, D. J., Marques, F. P. L. & Lahr, D. J. G. Genome skimming is a low-cost and robust strategy to assemble complete mitochondrial genomes from ethanol preserved specimens in biodiversity studies. PeerJ 7, e7543. https://doi.org/10.7717/peerj.7543 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Franco-Sierra, N. D. & Díaz-Nieto, J. F. Rapid mitochondrial genome sequencing based on Oxford Nanopore Sequencing and a proxy for vertebrate species identification. Ecol. Evol. 10, 3544–3560 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Baeza, J. A. Yes, we can use it: a formal test on the accuracy of low-pass nanopore long-read sequencing for mitophylogenomics and barcoding research using the Caribbean spiny lobster Panulirus argus. BMC Genomics 21, 882. https://doi.org/10.1186/s12864-020-07292-5 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Phillips, A. R., Robertson, A. L., Batzli, J., Harris, M. & Miller, S. Aligning goals, assessments, and activities: An approach to teaching PCR and gel electrophoresis. CBE Life Sci. Educ. 7, 96–106 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dhorne-Pollet, S., Barrey, E. & Pollet, N. A new method for long-read sequencing of animal mitochondrial genomes: application to the identification of equine mitochondrial DNA variants. BMC Genomics 21, 785. https://doi.org/10.1186/s12864-020-07183-9 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jain, M., Olsen, H. E., Paten, B. & Akeson, M. The Oxford Nanopore MinION: Delivery of nanopore sequencing to the genomics community. Genome Biol. 17, 239. https://doi.org/10.1186/s13059-016-1103-0 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Krehenwinkel, H. et al. Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale. GigaScience 8, giz006. https://doi.org/10.1093/gigascience/giz006 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Srivathsan, A. et al. ONTbarcoder and MinION barcodes aid biodiversity discovery and identification by everyone, for everyone. BMC Biol. 19, 217. https://doi.org/10.1186/s12915-021-01141-x (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Prost, S. et al. Education in the genomics era: Generating high-quality genome assemblies in university courses. GigaScience 9, giaa058. https://doi.org/10.1093/gigascience/giaa058 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Salazar, A. N. et al. An educational guide for nanopore sequencing in the classroom. PLoS Comput. Biol. 16, e1007314. https://doi.org/10.1371/journal.pcbi.1007314 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Watsa, M., Erkenswick, G. A., Pomerantz, A. & Prost, S. Portable sequencing as a teaching tool in conservation and biodiversity research. PLoS Biol. 18, e3000667. https://doi.org/10.1371/journal.pbio.3000667 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Egeter, B. et al. Speeding up the detection of invasive bivalve species using environmental DNA: A Nanopore and Illumina sequencing comparison. Mol. Ecol. Resour. https://doi.org/10.1111/1755-0998.13610 (2022).Article 
    PubMed 

    Google Scholar 
    Oxford Nanopore. Flongle. https://nanoporetech.com/products/flongle. Last accessed 05 May 2022 (2022).Oxford Nanopore. MinION. https://nanoporetech.com/products/minion. Last accessed 05 May 2022 (2022).Baeza, J. A. & García-De León, F. J. Are we there yet? Benchmarking low-coverage nanopore long-read sequencing for the assembling of mitochondrial genomes using the vulnerable silky shark Carcharhinus falciformis. BMC Genomics 23, 320. https://doi.org/10.1186/s12864-022-08482-z (2022).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ghiselli, F. et al. Molluscan mitochondrial genomes break the rules. Philos. Trans. R. Soc. B Biol. Sci. 376, 20200159. https://doi.org/10.1098/rstb.2020.0159 (2021).Article 

    Google Scholar 
    Zhang, Z.-Q. Animal biodiversity: An introduction to higher-level classification and taxonomic richness. Zootaxa 3148, 7–12 (2011).Article 

    Google Scholar 
    Bouchet, P., Bary, S., Héros, V. & Marani, G. How many species of molluscs are there in the world’s oceans, and who is going to describe them? In Tropical Deep-Sea Benthos 29 (eds Héros, V. et al.) 9–24 (Muséum national d’histoire naturelle, 2016).
    Google Scholar 
    Reese, D. S. Palaikastro shells and bronze age purple-dye production in the Mediterranean Basin. Annu. Br. Sch. Athens 82, 201–206 (1987).Article 

    Google Scholar 
    Lardans, V. & Dissous, C. Snail control strategies for reduction of schistosomiasis transmission. Parasitol. Today 14, 413–417 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Baker, G. M. (ed.) Molluscs as Crop Pests. (CABI, 2002). https://doi.org/10.1079/9780851993201.0000Mannino, M. A. & Thomas, K. D. Depletion of a resource? The impact of prehistoric human foraging on intertidal mollusc communities and its significance for human settlement, mobility and dispersal. World Archaeol. 33, 452–474 (2002).Article 

    Google Scholar 
    Carter, R. The history and prehistory of pearling in the Persian Gulf. J. Econ. Soc. Hist. Orient 48, 139–209 (2005).Article 

    Google Scholar 
    Vilariño, M. L. et al. Assessment of human enteric viruses in cultured and wild bivalve molluscs. Int. Microbiol. Off. J. Span. Soc. Microbiol. 12, 145–151 (2009).
    Google Scholar 
    Tedde, T. et al. Toxoplasma gondii and other zoonotic protozoans in Mediterranean mussel (Mytilus galloprovincialis) and blue mussel (Mytilus edulis): A food safety concern?. J. Food Prot. 82, 535–542 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 44, D67–D72 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Grande, C., Templado, J. & Zardoya, R. Evolution of gastropod mitochondrial genome arrangements. BMC Evol. Biol. 8, 61. https://doi.org/10.1186/1471-2148-8-61 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Formenti, G. et al. Complete vertebrate mitogenomes reveal widespread repeats and gene duplications. Genome Biol. 22, 120. https://doi.org/10.1186/s13059-021-02336-9 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Buchfink, B., Reuter, K. & Drost, H.-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540–546 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Meng, G., Li, Y., Yang, C. & Liu, S. MitoZ: A toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Res. 47, e63. https://doi.org/10.1093/nar/gkz173 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bernt, M. et al. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69, 313–319 (2013).PubMed 
    Article 

    Google Scholar 
    Chaisson, M. J. P., Wilson, R. K. & Eichler, E. E. Genetic variation and the de novo assembly of human genomes. Nat. Rev. Genet. 16, 627–640 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Alexander, J. & Valdés, A. The ring doesn’t mean a thing: Molecular data suggest a new taxonomy for two pacific species of sea hares (Mollusca: Opisthobranchia, Aplysiidae). Pac. Sci. 67, 283–294 (2013).Article 

    Google Scholar 
    WoRMS Editorial Board. World Register of Marine Species. https://www.marinespecies.org at VLIZ. Accessed 10 Jan 2022 (2022).Barco, A. et al. A molecular phylogenetic framework for the Muricidae, a diverse family of carnivorous gastropods. Mol. Phylogenet. Evol. 56, 1025–1039 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Houart, R. Description of eight new species and one new genus of Muricidae (Gastropoda) from the Indo-West Pacific. Novapex 18, 81–103 (2017).
    Google Scholar 
    Shao, K.-T. & Chung, K.-F. The National Checklist of Taiwan (Catalogue of Life in Taiwan, TaiCoL). GBIF. https://www.gbif.org/dataset/1ec61203-14fa-4fbd-8ee5-a4a80257b45a (2021).Gaitán-Espitia, J. D., González-Wevar, C. A., Poulin, E. & Cardenas, L. Antarctic and sub-Antarctic Nacella limpets reveal novel evolutionary characteristics of mitochondrial genomes in Patellogastropoda. Mol. Phylogenet. Evol. 131, 1–7 (2019).PubMed 
    Article 
    CAS 

    Google Scholar 
    Feng, J. et al. Comparative analysis of the complete mitochondrial genomes in two limpets from Lottiidae (Gastropoda: Patellogastropoda): rare irregular gene rearrangement within Gastropoda. Sci. Rep. 10, 19277. https://doi.org/10.1038/s41598-020-76410-w (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xu, T., Qi, L., Kong, L. & Li, Q. Mitogenomics reveals phylogenetic relationships of Patellogastropoda (Mollusca, Gastropoda) and dynamic gene rearrangements. Zool. Scr. 51, 147–160 (2022).Article 

    Google Scholar 
    Ranjard, L. et al. Complete mitochondrial genome of the green-lipped mussel, Perna canaliculus (Mollusca: Mytiloidea), from long nanopore sequencing reads. Mitoch. DNA Part B 3, 175–176 (2018).Article 

    Google Scholar 
    Sun, J. et al. The Scaly-foot Snail genome and implications for the origins of biomineralised armour. Nat. Commun. 11, 1657. https://doi.org/10.1038/s41467-020-15522-3 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dixit, B., Vanhoozer, S., Anti, N. A., O’Connor, M. S. & Boominathan, A. Rapid enrichment of mitochondria from mammalian cell cultures using digitonin. MethodsX 8, 101197. https://doi.org/10.1016/j.mex.2020.101197 (2021).Article 
    PubMed 

    Google Scholar 
    Wanner, N., Larsen, P. A., McLain, A. & Faulk, C. The mitochondrial genome and Epigenome of the Golden lion Tamarin from fecal DNA using Nanopore adaptive sequencing. BMC Genomics 22, 726. https://doi.org/10.1186/s12864-021-08046-7 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Malukiewicz, J. et al. Genomic skimming and nanopore sequencing uncover cryptic hybridization in one of world’s most threatened primates. Sci. Rep. 11, 17279. https://doi.org/10.1038/s41598-021-96404-6 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kipp, E. J. et al. Nanopore adaptive sampling for mitogenome sequencing and bloodmeal identification in hematophagous insects. bioRxiv. https://doi.org/10.1101/2021.11.11.468279 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sereika, M. et al. Oxford Nanopore R10.4 long-read sequencing enables near-perfect bacterial genomes from pure cultures and metagenomes without short-read or reference polishing. bioRxiv. https://doi.org/10.1101/2021.10.27.466057 (2021).Article 

    Google Scholar 
    Oxford Nanopore. Nanopore Community. https://nanoporetech.com/community. Last accessed 05 May 2022 (2022).Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Li, H. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27, 737–746 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oxford Nanopore. medaka. https://github.com/nanoporetech/medaka. Last accessed 05 May 2022 (2022).Walker, B. J. et al. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9, e112963. https://doi.org/10.1371/journal.pone.0112963 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Faust, G. G. & Hall, I. M. SAMBLASTER: Fast duplicate marking and structural variant read extraction. Bioinformatics 30, 2503–2505 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pedersen, B. S. & Quinlan, A. R. Mosdepth: Quick coverage calculation for genomes and exomes. Bioinformatics 34, 867–868 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tsai, I. J. Genome skimming exercise (last updated 2022.04.14). https://introtogenomics.readthedocs.io/en/latest/emcgs.html (2022).Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vaidya, G., Lohman, D. J. & Meier, R. SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180 (2011).PubMed 
    Article 

    Google Scholar 
    Edler, D., Klein, J., Antonelli, A. & Silvestro, D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol. Evol. 12, 373–377 (2021).Article 

    Google Scholar 
    Rabiee, M., Sayyari, E. & Mirarab, S. Multi-allele species reconstruction using ASTRAL. Mol. Phylogenet. Evol. 130, 286–296 (2019).PubMed 
    Article 

    Google Scholar 
    Rambaut, A. FigTree, version 1.4.4. http://tree.bio.ed.ac.uk/software/figtree/ (2018).Hackl, T. & Ankenbrand, M. J. gggenomes: A Grammar of Graphics for Comparative Genomics. https://github.com/thackl/gggenomes (2022).Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Coronilla juncea, a native candidate for phytostabilization of potentially toxic elements and restoration of Mediterranean soils

    Pourret, O. & Hursthouse, A. It’s time to replace the term “heavy metals” with “potentially toxic elements” when reporting environmental research. IJERPH 16, 4446 (2019).CAS 
    PubMed Central 

    Google Scholar 
    Wuana, R. A. & Okieimen, F. E. Heavy metals in contaminated soils: A review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. 2011, 1–20 (2011).
    Google Scholar 
    Mahar, A. et al. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review. Ecotoxicol. Environ. Saf. 126, 111–121 (2016).CAS 
    PubMed 

    Google Scholar 
    Vangronsveld, J. et al. Phytoremediation of contaminated soils and groundwater: Lessons from the field. Environ. Sci. Pollut. Res. 16, 765–794 (2009).CAS 

    Google Scholar 
    Desjardins, D., Nissim, W. G., Pitre, F. E., Naud, A. & Labrecque, M. Distribution patterns of spontaneous vegetation and pollution at a former decantation basin in southern Québec, Canada. Ecol. Eng. 64, 385–390 (2014).
    Google Scholar 
    Marchiol, L. et al. Gentle remediation at the former “Pertusola Sud” zinc smelter: Evaluation of native species for phytoremediation purposes. Ecol. Eng. 53, 343–353 (2013).
    Google Scholar 
    van Oort, F. et al. Les pollutions métalliques d’un site industriel et des sols environnants : distributions hétérogènes des métaux et relations avec l’usage des sols. In: Contaminations métalliques des agrosystèmes et écosystèmes péri-urbains 15–44 (Editions Quae, 2009).Hodge, A. Plastic plants and patchy soils. J. Exp. Bot. 57, 401–411 (2006).CAS 
    PubMed 

    Google Scholar 
    Huber-Sannwald, E. & Jackson, R. B. Heterogeneous soil-resource distribution and plant responses—from individual-plant growth to ecosystem functioning. In Progress in Botany Vol. 62 (eds Esser, K. et al.) 451–476 (Springer, 2001).
    Google Scholar 
    Loecke, T. D. & Philip Robertson, G. Soil resource heterogeneity in the form of aggregated litter alters maize productivity. Plant Soil 325, 231–241 (2009).CAS 

    Google Scholar 
    Reynolds, H. L., Hungate, B. A., Iii, F. S. C. & D’Antonio, C. M. Soil Heterogeneity and Plant Competition in an Annual Grassland. 16 (2021).Maestre, F. T., Cortina, J., Bautista, S., Bellot, J. & Vallejo, R. Small-scale environmental heterogeneity and spatiotemporal dynamics of seedling establishment in a semiarid degraded ecosystem. Ecosystems 6, 630–643 (2003).
    Google Scholar 
    Shutcha, M. N. et al. Three years of phytostabilisation experiment of bare acidic soil extremely contaminated by copper smelting using plant biodiversity of metal-rich soils in tropical Africa (Katanga, DR Congo). Ecol. Eng. 82, 81–90 (2015).
    Google Scholar 
    Testiati, E. et al. Trace metal and metalloid contamination levels in soils and in two native plant species of a former industrial site: Evaluation of the phytostabilization potential. J. Hazard. Mater. 248–249, 131–141 (2013).PubMed 

    Google Scholar 
    Cabrera, F., Clemente, L., Díaz Barrientos, E., López, R. & Murillo, J. M. Heavy metal pollution of soils affected by the Guadiamar toxic fiood. Sci. Total Environ. 242, 117–129 (1999).CAS 
    PubMed 

    Google Scholar 
    Imperato, M. et al. Spatial distribution of heavy metals in urban soils of Naples city (Italy). Environ. Pollut. 124, 247–256 (2003).CAS 
    PubMed 

    Google Scholar 
    Gallagher, F. J., Pechmann, I., Bogden, J. D., Grabosky, J. & Weis, P. Soil metal concentrations and vegetative assemblage structure in an urban brownfield. Environ. Pollut. 153, 351–361 (2008).CAS 
    PubMed 

    Google Scholar 
    Gallagher, F. J., Pechmann, I., Holzapfel, C. & Grabosky, J. Altered vegetative assemblage trajectories within an urban brownfield. Environ. Pollut. 159, 1159–1166 (2011).CAS 
    PubMed 

    Google Scholar 
    Heckenroth, A. et al. Selection of native plants with phytoremediation potential for highly contaminated Mediterranean soil restoration: Tools for a non-destructive and integrative approach. J. Environ. Manag. 183, 850–863 (2016).CAS 

    Google Scholar 
    Dickinson, N. M., Turner, A. P. & Lepp, N. W. How do trees and other long-lived plants survive in polluted environments?. Funct. Ecol. 5, 5 (1991).
    Google Scholar 
    Partida-Martínez, L. P. & Heil, M. The microbe-free plant: Fact or artifact?. Front. Plant Sci. 2, 100 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Giller, K. E., Witter, E. & Mcgrath, S. P. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: A review. Soil Biol. Biochem. 30, 1389–1414 (1998).CAS 

    Google Scholar 
    Kabata-Pendias, A. & Pendias, H. Trace Elements in Soils and Plants (CRC Press, 2001).
    Google Scholar 
    Tyler, G. Heavy metal pollution and mineralisation of nitrogen in forest soils. Nature 255, 701–702 (1975).CAS 

    Google Scholar 
    Seshadri, B., Bolan, N. S. & Naidu, R. Rhizosphere-induced heavy metal(loid) transformation in relation to bioavailability and remediation. J. Soil Sci. Plant Nutr. https://doi.org/10.4067/S0718-95162015005000043 (2015).Article 

    Google Scholar 
    Kidd, P. et al. Trace element behaviour at the root–soil interface: Implications in phytoremediation. Environ. Exp. Bot. 67, 243–259 (2009).CAS 

    Google Scholar 
    Rivera-Becerril, F. Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J. Exp. Bot. 53, 1177–1185 (2002).CAS 
    PubMed 

    Google Scholar 
    Krupa, P. & Kozdrój, J. Ectomycorrhizal fungi and associated bacteria provide protection against heavy metals in inoculated pine (Pinus sylvestris L.) seedlings. Water Air Soil Pollut. 182, 83–90 (2007).CAS 

    Google Scholar 
    Janoušková, M., Pavlíková, D. & Vosátka, M. Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil. Chemosphere 65, 1959–1965 (2006).PubMed 

    Google Scholar 
    Leyval, C., Turnau, K. & Haselwandter, K. Effect of heavy metal pollution on mycorrhizal colonization and function: Physiological, ecological and applied aspects. Mycorrhiza 7, 139–153 (1997).CAS 

    Google Scholar 
    Zhang, Y., Zhang, Y., Liu, M., Shi, X. & Zhao, Z. Dark septate endophyte (DSE) fungi isolated from metal polluted soils: Their taxonomic position, tolerance, and accumulation of heavy metals in vitro. J. Microbiol. 46, 624–632 (2008).PubMed 

    Google Scholar 
    Krumins, J. A., Goodey, N. M. & Gallagher, F. Plant–soil interactions in metal contaminated soils. Soil Biol. Biochem. 80, 224–231 (2015).CAS 

    Google Scholar 
    Glick, B. R. Phytoremediation: Synergistic use of plants and bacteria to clean up the environment. Biotechnol. Adv. 21, 383–393 (2003).CAS 
    PubMed 

    Google Scholar 
    Heckenroth, A. et al. What are the potential environmental solutions for diffuse pollution ? In Pollution of Marseille’s Industrial Calanques—The Impact of the Past on the Present 291–328 (REF2C, 2016).Li, M. S. Ecological restoration of mineland with particular reference to the metalliferous mine wasteland in China: A review of research and practice. Sci. Total Environ. 357, 38–53 (2006).CAS 
    PubMed 

    Google Scholar 
    Mendez, M. O. & Maier, R. M. Phytoremediation of mine tailings in temperate and arid environments. Rev. Environ. Sci. Biotechnol. 7, 47–59 (2008).CAS 

    Google Scholar 
    Yaalon, D. H. Soils in the Mediterranean region: What makes them different?. CATENA 28, 157–169 (1997).CAS 

    Google Scholar 
    Li, S. et al. A comprehensive survey on the horizontal and vertical distribution of heavy metals and microorganisms in soils of a Pb/Zn smelter. J. Hazard. Mater. 400, 123255 (2020).CAS 
    PubMed 

    Google Scholar 
    Pérez-de-Mora, A. et al. Microbial community structure and function in a soil contaminated by heavy metals: Effects of plant growth and different amendments. Soil Biol. Biochem. 38, 327–341 (2006).
    Google Scholar 
    Keller, C. et al. Root development and heavy metal phytoextraction efficiency: Comparison of different plant species in the field. Plant Soil. 249, 67–81 (2003).CAS 

    Google Scholar 
    Lambrechts, T. et al. Comparative analysis of Cd and Zn impacts on root distribution and morphology of Lolium perenne and Trifolium repens: Implications for phytostabilization. Plant Soil 376, 229–244 (2014).CAS 

    Google Scholar 
    Pauwels, M., Frérot, H., Bonnin, I. & Saumitou-Laprade, P. A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J. Evol. Biol. 19, 1838–1850 (2006).CAS 
    PubMed 

    Google Scholar 
    Padilla, F. M. & Pugnaire, F. I. The role of nurse plants in the restoration of degraded environments. Front. Ecol. Environ. 4, 196–202 (2006).
    Google Scholar 
    Robles, A. B., Allegretti, L. I. & Passera, C. B. Coronilla juncea is both a nutritive fodder shrub and useful in the rehabilitation of abandoned Mediterranean marginal farmland. J. Arid Environ. 50, 381–392 (2002).
    Google Scholar 
    Grime, J. P. Plant Strategies and Vegetation Processes (Wiley, 1979).
    Google Scholar 
    Laffont-Schwob, I. et al. Diffuse and widespread present-day pollution. In Pollution of Marseille’s industrial Calanques—The Impact of the Past on the Future 204–249 (REF2C, 2016).Gelly, R. et al. Lead, zinc, and copper redistributions in soils along a deposition gradient from emissions of a Pb-Ag smelter decommissioned 100 years ago. Sci. Total Environ. 665, 502–512 (2019).CAS 
    PubMed 

    Google Scholar 
    Tóth, G. et al. Soils of the European Union. JRC Scientific and Technical Reports 85 (2008).IUSS Working Group WRB. Base de référence mondiale pour les ressources en sols 2014, Mise à jour 2015. Système international de classification des sols pour nommer les sols et élaborer des légendes de cartes pédologiques. Rapport sur les ressources en sols du monde. Vol. 106 (2015).Dias, T. et al. Ammonium as a driving force of plant diversity and ecosystem functioning: Observations based on 5 years’ manipulation of n dose and form in a Mediterranean ecosystem. PLoS ONE 9, e92517 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Remon, E. et al. Soil characteristics, heavy metal availability and vegetation recovery at a former metallurgical landfill: Implications in risk assessment and site restoration. Environ. Pollut. 137, 316–323 (2005).CAS 
    PubMed 

    Google Scholar 
    Baumberger, T. et al. Plant community changes as ecological indicator of seabird colonies’ impacts on Mediterranean Islands. Ecol. Ind. 15, 76–84 (2012).
    Google Scholar 
    Navas, M.-L., Roumet, C., Bellmann, A., Laurent, G. & Garnier, E. Suites of plant traits in species from different stages of a Mediterranean secondary succession: Plant traits and succession. Plant Biol. 12, 183–196 (2010).CAS 
    PubMed 

    Google Scholar 
    Guillamot, F., Calvert, V., Millot, M.-V. & Criquet, S. Does antimony affect microbial respiration in Mediterranean soils? A microcosm experiment. Pedobiologia 57, 119–121 (2014).
    Google Scholar 
    Wang, A., He, M., Ouyang, W., Lin, C. & Liu, X. Effects of antimony (III/V) on microbial activities and bacterial community structure in soil. Sci. Total Environ. 789, 148073 (2021).CAS 
    PubMed 

    Google Scholar 
    Oleńska, E. et al. Trifolium repens-associated bacteria as a potential tool to facilitate phytostabilization of zinc and lead polluted waste heaps. Plants 9, 1002 (2020).PubMed Central 

    Google Scholar 
    Stambulska, U. Y., Bayliak, M. M. & Lushchak, V. I. Chromium(VI) toxicity in legume plants: Modulation effects of rhizobial symbiosis. BioMed Res. Int. 2018, 1–13 (2018).
    Google Scholar 
    Karthika, K. S., Rashmi, I. & Parvathi, M. S. Biological functions, uptake and transport of essential nutrients in relation to plant growth. In Plant Nutrients and Abiotic Stress Tolerance 1–49 (Springer Singapore, 2018). https://doi.org/10.1007/978-981-10-9044-8_1.Dary, M., Chamber-Pérez, M. A., Palomares, A. J. & Pajuelo, E. “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J. Hazard. Mater. 177, 323–330 (2010).CAS 
    PubMed 

    Google Scholar 
    Reichman, S. M. The potential use of the legume–rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biol. Biochem. 39, 2587–2593 (2007).CAS 

    Google Scholar 
    Parraga-Aguado, I., Querejeta, J.-I., González-Alcaraz, M.-N., Jiménez-Cárceles, F. J. & Conesa, H. M. Usefulness of pioneer vegetation for the phytomanagement of metal(loid)s enriched tailings: Grasses vs. shrubs vs. trees. J. Environ. Manag. 133, 51–58 (2014).CAS 

    Google Scholar 
    Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373 (1994).
    Google Scholar 
    Carrasco, L., Azcón, R., Kohler, J., Roldán, A. & Caravaca, F. Comparative effects of native filamentous and arbuscular mycorrhizal fungi in the establishment of an autochthonous, leguminous shrub growing in a metal-contaminated soil. Sci. Total Environ. 409, 1205–1209 (2011).CAS 
    PubMed 

    Google Scholar 
    Padilla, F. M., Ortega, R., Sánchez, J. & Pugnaire, F. I. Rethinking species selection for restoration of arid shrublands. Basic Appl. Ecol. 10, 640–647 (2009).
    Google Scholar 
    Ilunga wa Ilunga, E. et al. Plant functional traits as a promising tool for the ecological restoration of degraded tropical metal-rich habitats and revegetation of metal-rich bare soils: A case study in copper vegetation of Katanga, DRC. Ecol. Eng. 82, 214–221 (2015).
    Google Scholar 
    Salducci, M.-D. et al. How can a rare protected plant cope with the metal and metalloid soil pollution resulting from past industrial activities? Phytometabolites, antioxidant activities and root symbiosis involved in the metal tolerance of Astragalus tragacantha. Chemosphere 217, 887–896 (2019).CAS 
    PubMed 

    Google Scholar 
    Kachout, S. S. et al. Accumulation of Cu, Pb, Ni and Zn in the halophyte plant Atriplex grown on polluted soil. J. Sci. Food Agric. 92, 336–342 (2012).CAS 
    PubMed 

    Google Scholar 
    Schaeffer, A. et al. The impact of chemical pollution on the resilience of soils under multiple stresses: A conceptual framework for future research. Sci. Total Environ. 568, 1076–1085 (2016).CAS 
    PubMed 

    Google Scholar 
    Tosini, L. et al. Gain in biodiversity but not in phytostabilization after 3 years of ecological restoration of contaminated Mediterranean soils. Ecol. Eng. 157, 105998 (2020).
    Google Scholar 
    Michelaki, C. et al. An integrated phenotypic trait-network in thermo-Mediterranean vegetation describing alternative, coexisting resource-use strategies. Sci. Total Environ. 672, 583–592 (2019).CAS 
    PubMed 

    Google Scholar 
    Affholder, M.-C. et al. Transfer of metals and metalloids from soil to shoots in wild rosemary (Rosmarinus officinalis L.) growing on a former lead smelter site: Human exposure risk. Sci. Total Environ. 454–455, 219–229 (2013).PubMed 

    Google Scholar 
    Affholder, M.-C. et al. As, Pb, Sb, and Zn transfer from soil to root of wild rosemary: Do native symbionts matter?. Plant Soil 382, 219–236 (2014).CAS 

    Google Scholar 
    Ellili, A. et al. Decision-making criteria for plant-species selection for phytostabilization: Issues of biodiversity and functionality. J. Environ. Manag. 201, 215–226 (2017).CAS 

    Google Scholar 
    Laffont-Schwob, I. et al. Insights on metal-tolerance and symbionts of the rare species Astragalus tragacantha aiming at phytostabilization of polluted soils and plant conservation. ecmed 37, 57–62 (2011).
    Google Scholar 
    Rabier, J. et al. Heavy metal and arsenic resistance of the halophyte Atriplex halimus L. along a gradient of contamination in a French Mediterranean spray zone. Water Air Soil Pollut. 225, 1993 (2014).
    Google Scholar 
    Quevauviller, Ph. et al. Interlaboratory comparison of EDTA and DTPA procedures prior to certification of extractable trace elements in calcareous soil. Sci. Total Environ. 178, 127–132 (1996).CAS 

    Google Scholar 
    Anderson, J. P. E. & Domsch, K. H. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221 (1978).CAS 

    Google Scholar 
    R Development Core Team.pdf.Dray, S., Dufour, A. B. & Chessel, D. The ade4 package—II: Two-table and K-table methods. R News 7, 6 (2007).
    Google Scholar  More

  • in

    Behavioural and neural responses of crabs show evidence for selective attention in predator avoidance

    Faisal, A. A., Selen, L. P. J. & Wolpert, D. M. Noise in the nervous system. Nat. Rev. Neurosci. 9, 292–303 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tsetsos, K. et al. Economic irrationality is optimal during noisy decision making. Proc. Natl. Acad. Sci. 113, 3102–3107 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bushnell, P. J. Behavioral approaches to the assessment of attention in animals. Psychopharmacology 138, 231–259 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Katsuki, F. & Constantinidis, C. Bottom-up and top-down attention: Different processes and overlapping neural systems. Neuroscientist 20, 509–521 (2014).PubMed 
    Article 

    Google Scholar 
    Moore, T. & Zirnsak, M. Neural mechanisms of selective visual attention. Annu. Rev. Psychol. 68, 47–72 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ferguson, K. I. & Stiling, P. Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108, 375–379 (1996).ADS 
    PubMed 
    Article 

    Google Scholar 
    Sih, A., Englund, G. & Wooster, D. Emergent impacts of multiple predators on prey. Trends Ecol. Evol. 13, 350–355 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Soluk, D. A. & Collins, N. C. Synergistic interactions between fish and stoneflies: Facilitation and interference among stream predators. Oikos. 52, 94–100 (1988).
    Article 

    Google Scholar 
    Cooper, W. E., Pérez-Mellado, V. & Hawlena, D. Number, speeds, and approach paths of predators affect escape behavior by the Balearic lizard, Podarcis lilfordi. J. Herpetol. 41, 197–204 (2007).Article 

    Google Scholar 
    Relyea, R. A. How prey respond to combined predators: A review and an empirical test. Ecology 84, 1827–1839 (2003).Article 

    Google Scholar 
    Krupa, J. J. & Sih, A. Fishing spiders, green sunfish, and a stream-dwelling water strider: Male–female conflict and prey responses to single versus multiple predator environments. Oecologia 117, 258–265 (1998).ADS 
    PubMed 
    Article 

    Google Scholar 
    Nityananda, V. Attention-like processes in insects. Proc. R. Soc. B Biol. Sci. 283, 20161986 (2016).Article 

    Google Scholar 
    Amo, L., López, P. & Martín, J. in Annales Zoologici Fennici, 671–679 (JSTOR).Bagheri, Z. M., Donohue, C. G. & Hemmi, J. M. Evidence of predictive selective attention in fiddler crabs during escape in the natural environment. J. Exp. Biol. 223, 234963 (2020).Article 

    Google Scholar 
    Geist, C., Liao, J., Libby, S. & Blumstein, D. T. Does intruder group size and orientation affect flight initiation distance in birds?. Anim. Biodivers. Conserv. 28, 69–73 (2005).
    Google Scholar 
    McIntosh, A. R. & Peckarsky, B. L. Criteria determining behavioural responses to multiple predators by a stream mayfly. Oikos. 554–564 (1999).Hemmi, J. M. & Tomsic, D. The neuroethology of escape in crabs: From sensory ecology to neurons and back. Curr. Opin. Neurobiol. 22, 194–200 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Zeil, J. & Hemmi, J. M. The visual ecology of fiddler crabs. J. Comp. Physiol. A. 192, 1–25 (2006).ADS 
    Article 

    Google Scholar 
    Nalbach, H.-O., Nalbach, G. & Forzin, L. Visual control of eye-stalk orientation in crabs: Vertical optokinetics, visual fixation of the horizon, and eye design. J. Comp. Physiol. A. 165, 577–587 (1989).Article 

    Google Scholar 
    Zeil, J. & Al-Mutairi, M. The variation of resolution and of ommatidial dimensions in the compound eyes of the fiddler crab Uca lactea annulipes (Ocypodidae, Brachyura, Decapoda). J. Exp. Biol. 199, 1569–1577 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    Howard, J. & Snyder, A. W. Transduction as a limitation on compound eye function and design. Proc. R. Soc. Lond. Series B Biol. Sci. 217, 287–307 (1983).ADS 

    Google Scholar 
    Land, M. F. Visual acuity in insects. Annu. Rev. Entomol. 42, 147–177 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    Land, M. F. & Nilsson, D.-E. Animal Eyes (OUP, 2012).Book 

    Google Scholar 
    Bagheri, Z. M. et al. A new method for mapping spatial resolution in compound eyes suggests two visual streaks in fiddler crabs. J. Exp. Biol. 223, 210195 (2020).Article 

    Google Scholar 
    Smolka, J. & Hemmi, J. M. Topography of vision and behaviour. J. Exp. Biol. 212, 3522–3532 (2009).PubMed 
    Article 

    Google Scholar 
    Land, M. & Layne, J. The visual control of behaviour in fiddler crabs. J. Comp. Physiol. A. 177, 91–103 (1995).Article 

    Google Scholar 
    Layne, J., Land, M. & Zeil, J. Fiddler crabs use the visual horizon to distinguish predators from conspecifics: A review of the evidence. J. Mar. Biol. Assoc. UK. 77, 43–54 (1997).Article 

    Google Scholar 
    Hemmi, J. M. Predator avoidance in fiddler crabs: 1. Escape decisions in relation to the risk of predation. Animal Behav. 69, 603–614 (2005).Article 

    Google Scholar 
    Layne, J. E. Retinal location is the key to identifying predators in fiddler crabs (Uca pugilator). J. Exp. Biol. 201, 2253–2261 (1998).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nalbach, H.-O. Frontiers in Crustacean Neurobiology 165–172 (Springer, 1990).Book 

    Google Scholar 
    Smolka, J., Zeil, J. & Hemmi, J. M. Natural visual cues eliciting predator avoidance in fiddler crabs. Proc. R. Soc. B Biol. Sci. 278, 3584–3592 (2011).Article 

    Google Scholar 
    Hemmi, J. M. Predator avoidance in fiddler crabs: 2. The visual cues. Animal Behav. 69, 615–625 (2005).Article 

    Google Scholar 
    Hemmi, J. M. & Pfeil, A. A multi-stage anti-predator response increases information on predation risk. J. Exp. Biol. 213, 1484–1489 (2010).PubMed 
    Article 

    Google Scholar 
    Smolka, J., Raderschall, C. A. & Hemmi, J. M. Flicker is part of a multi-cue response criterion in fiddler crab predator avoidance. J. Exp. Biol. 216, 1219–1224 (2013).PubMed 

    Google Scholar 
    How, M. J., Pignatelli, V., Temple, S. E., Marshall, N. J. & Hemmi, J. M. High e-vector acuity in the polarisation vision system of the fiddler crab Uca vomeris. J. Exp. Biol. 215, 2128–2134 (2012).PubMed 
    Article 

    Google Scholar 
    Paulk, A. C. et al. Selective attention in the honeybee optic lobes precedes behavioral choices. Proc. Natl. Acad. Sci. 111, 5006–5011 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tang, S. & Juusola, M. Intrinsic activity in the fly brain gates visual information during behavioral choices. Nat. Precedings. 1–1 (2010).Bagheri, Z. M., Cazzolato, B. S., Grainger, S., O’Carroll, D. C. & Wiederman, S. D. An autonomous robot inspired by insect neurophysiology pursues moving features in natural environments. J. Neural Eng. 14, 046030 (2017).ADS 
    PubMed 
    Article 

    Google Scholar 
    Chancán, M., Hernandez-Nunez, L., Narendra, A., Barron, A. B. & Milford, M. A hybrid compact neural architecture for visual place recognition. IEEE Robot. Automat. Lett. 5, 993–1000 (2020).Article 

    Google Scholar 
    Colonnier, F., Ramirez-Martinez, S., Viollet, S. & Ruffier, F. A bio-inspired sighted robot chases like a hoverfly. Bioinspir. Biomim. 14, 036002 (2019).ADS 
    PubMed 
    Article 

    Google Scholar 
    Medan, V., Oliva, D. & Tomsic, D. Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus. J. Neurophysiol. 98, 2414–2428 (2007).PubMed 
    Article 

    Google Scholar 
    Oliva, D. & Tomsic, D. Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice. J. Neurophysiol. 112, 1477–1490 (2014).PubMed 
    Article 

    Google Scholar 
    Oliva, D. & Tomsic, D. Object approach computation by a giant neuron and its relationship with the speed of escape in the crab Neohelice. J. Exp. Biol. 219, 3339–3352 (2016).PubMed 

    Google Scholar 
    Sztarker, J., Strausfeld, N. J. & Tomsic, D. Organization of optic lobes that support motion detection in a semiterrestrial crab. J. Comparat. Neurol. 493, 396–411 (2005).Article 

    Google Scholar 
    Medan, V., De Astrada, M. B., Scarano, F. & Tomsic, D. A network of visual motion-sensitive neurons for computing object position in an arthropod. J. Neurosci. 35, 6654–6666 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tomsic, D. & Sztarker, J. in Oxford Research Encyclopedia of Neuroscience (2019).Sztarker, J. & Tomsic, D. Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations. J. Comp. Physiol. A. 194, 587–596 (2008).Article 

    Google Scholar 
    Tomsic, D., de Astrada, M. B. & Sztarker, J. Identification of individual neurons reflecting short-and long-term visual memory in an arthropodo. J. Neurosci. 23, 8539–8546 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Layne, J. E., Barnes, W. J. P. & Duncan, L. M. J. Mechanisms of homing in the fiddler crab Uca rapax 1. Spatial and temporal characteristics of a system of small-scale navigation. J. Exp. Biol. 206, 4413–4423 (2003).PubMed 
    Article 

    Google Scholar 
    Dahmen, H., Wahl, V. L., Pfeffer, S. E., Mallot, H. A. & Wittlinger, M. Naturalistic path integration of Cataglyphis desert ants on an air-cushioned lightweight spherical treadmill. J. Exp. Biol. 220, 634–644 (2017).PubMed 
    Article 

    Google Scholar 
    Hemmi, J. M. & Merkle, T. High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc. R. Soc. B Biol. Sci. 276, 4381–4388 (2009).Article 

    Google Scholar 
    Scarano, F. & Tomsic, D. Escape response of the crab Neohelice to computer generated looming and translational visual danger stimuli. J. Physiol.-Paris 108, 141–147 (2014).PubMed 
    Article 

    Google Scholar 
    Ryan, T. P. & Morgan, J. P. Modern experimental design. J. Stat. Theory Practice 1, 501–506 (2007).MATH 
    Article 

    Google Scholar 
    Hemmi, J. M. & Zeil, J. Burrow surveillance in fiddler crabs I. Description of behaviour. J. Exp. Biol. 206, 3935–3950 (2003).PubMed 
    Article 

    Google Scholar 
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. (2014).emmeans: Estimated Marginal Means, aka Least-Squares Means. v. R package version 1.5.2-1. (2020).Cremers, J. Bpnreg: Bayesian projected normal regression models for circular data. R Package Version 1, 3 (2018).
    Google Scholar 
    Cremers, J. & Klugkist, I. One direction? A tutorial for circular data analysis using R with examples in cognitive psychology. Front. Psychol. 2040 (2018).Oliva, D., Medan, V. & Tomsic, D. Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae). J. Exp. Biol. 210, 865–880 (2007).PubMed 
    Article 

    Google Scholar 
    Gabbiani, F., Krapp, H. G. & Laurent, G. Computation of object approach by a wide-field, motion-sensitive neuron. J. Neurosci. 19, 1122–1141 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Simultaneous Inference in General Parametric Models. v. R package version v1.4-10 (2019).Avargues-Weber, A., Deisig, N. & Giurfa, M. Visual cognition in social insects. Annu. Rev. Entomol. 56, 423–443 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Avarguès-Weber, A. & Giurfa, M. Conceptual learning by miniature brains. Proc. R. Soc. B Biol. Sci. 280, 20131907 (2013).Article 

    Google Scholar 
    De Bivort, B. L. & Van Swinderen, B. Evidence for selective attention in the insect brain. Curr. Opin. Insect Sci. 15, 9–15 (2016).PubMed 
    Article 

    Google Scholar 
    Klapoetke, N. C. et al. Ultra-selective looming detection from radial motion opponency. Nature 551, 237–241 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Von Reyn, C. R. et al. A spike-timing mechanism for action selection. Nat. Neurosci. 17, 962–970 (2014).Article 
    CAS 

    Google Scholar 
    Fotowat, H. & Gabbiani, F. Collision detection as a model for sensory-motor integration. Annu. Rev. Neurosci. 34, 1–19 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Strausfeld, N. J. & Olea-Rowe, B. Convergent evolution of optic lobe neuropil in Pancrustacea. Arthropod. Struct. Dev. 61, 101040 (2021).PubMed 
    Article 

    Google Scholar 
    Tomsic, D. Visual motion processing subserving behavior in crabs. Curr. Opin. Neurobiol. 41, 113–121 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Giribet, G. & Edgecombe, G. D. The phylogeny and evolutionary history of arthropods. Curr. Biol. 29, R592–R602 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Christian, E. V. Sprung der Collembolen. Zoologische Jahrbucher. Abteilung fur Systematik, Okologie und Geographie der Tiere (1979).Brackenbury, J. Regulation of swimming in the Culex pipiens (Diptera, Culicidae) pupa: Kinematics and locomotory trajectories. J. Exp. Biol. 202, 2521–2529 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Domenici, P. & Blake, R. W. Escape trajectories in angelfish (Pterophyllum eimekei). J. Exp. Biol. 177, 253–272 (1993).Article 

    Google Scholar 
    Kimura, H. & Kawabata, Y. Effect of initial body orientation on escape probability of prey fish escaping from predators. Biol. Open. 7, bio023812 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Martín, J. & López, P. The escape response of juvenile Psammodromus algirus lizards. J. Comp. Psychol. 110, 187 (1996).Article 

    Google Scholar 
    Lancer, B. H., Evans, B. J. E., Fabian, J. M., O’Carroll, D. C. & Wiederman, S. D. A target-detecting visual neuron in the dragonfly locks on to selectively attended targets. J. Neurosci. 39, 8497–8509 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nityananda, V. & Pattrick, J. G. Bumblebee visual search for multiple learned target types. J. Exp. Biol. 216, 4154–4160 (2013).PubMed 

    Google Scholar 
    Pollack, G. S. Selective attention in an insect auditory neuron. J. Neurosci. 8, 2635–2639 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rossel, S. Binocular vision in insects: How mantids solve the correspondence problem. Proc. Natl. Acad. Sci. 93, 13229–13232 (1996).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Wiederman, S. D. & O’Carroll, D. C. Selective attention in an insect visual neuron. Curr. Biol. 23, 156–161 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Jackson, R. R. & Cross, F. R. Spider cognition. Adv. Insect Physiol. 41, 115–174 (2011).Article 

    Google Scholar 
    Jackson, R. R. & Li, D. One-encounter search-image formation by araneophagic spiders. Anim. Cogn. 7, 247–254 (2004).PubMed 
    Article 

    Google Scholar 
    Guest, B. B. & Gray, J. R. Responses of a looming-sensitive neuron to compound and paired object approaches. J. Neurophysiol. 95, 1428–1441 (2006).PubMed 
    Article 

    Google Scholar 
    Eliassen, S., Jørgensen, C., Mangel, M. & Giske, J. Quantifying the adaptive value of learning in foraging behavior. Am. Nat. 174, 478–489 (2009).PubMed 
    Article 

    Google Scholar 
    Eliassen, S., Andersen, B. S., Jørgensen, C. & Giske, J. From sensing to emergent adaptations: Modelling the proximate architecture for decision-making. Ecol. Model. 326, 90–100 (2016).Article 

    Google Scholar 
    Gigerenzer, G. Why heuristics work. Perspect. Psychol. Sci. 3, 20–29 (2008).PubMed 
    Article 

    Google Scholar  More

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    Stocking density mediated stress modulates growth attributes in cage reared Labeo rohita (Hamilton) using multifarious biomarker approach

    Tolussi, C. E., Hilsdorf, A. W. S., Caneppele, D. & Moreira, R. G. The effects of stocking density in physiological parameters and growth of the endangered teleost species piabanha, Brycon insignis (Steindachner, 1877). Aquaculture 310, 221–228 (2010).
    Google Scholar 
    Wang, Y. et al. Effects of stocking density on growth, serum parameters, antioxidant status, liver and intestine histology and gene expression of largemouth bass (Micropterus salmoides) farmed in the in-pond raceway system. Aquac. Res. 51, 5228–5240 (2020).CAS 

    Google Scholar 
    Zahedi, S., Akbarzadeh, A., Mehrzad, J., Noori, A. & Harsij, M. Effect of stocking density on growth performance, plasma biochemistry and muscle gene expression in rainbow trout (Oncorhynchus mykiss). Aquaculture 498, 271–278 (2019).CAS 

    Google Scholar 
    Yousefi, M., Paktinat, M., Mahmoudi, N., Pérez-Jiménez, A. & Hoseini, S. M. Serum biochemical and non-specific immune responses of rainbow trout (Oncorhynchus mykiss) to dietary nucleotide and chronic stress. Fish Physiol. Biochem. 42, 1417–1425 (2016).CAS 
    PubMed 

    Google Scholar 
    Duan, Y., Dong, X., Zhang, X. & Miao, Z. Effects of dissolved oxygen concentration and stocking density on the growth, energy budget and body composition of juvenile Japanese flounder, Paralichthys olivaceus (Temminck et Schlegel). Aquac. Res. 42, 407–416 (2011).CAS 

    Google Scholar 
    Castillo-Vargasmachuca, S. et al. Effect of stocking density on growth performance and yield of subadult pacific red snapper cultured in floating sea cages. N. Am. J. Aquac. 74, 413–418 (2012).
    Google Scholar 
    Upadhyay, A. et al. Stocking density matters in open water cage culture: influence on growth, digestive enzymes, haemato-immuno and stress responses of Puntius sarana (Ham, 1822). Aquaculture 547, 737445 (2021).
    Google Scholar 
    Kumar, V. et al. Assessment of the effect of sub-lethal acute toxicity of Emamectin benzoate in Labeo rohita using multiple biomarker approach. Toxicol. Rep. 9, 102–110 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rebl, A. et al. The synergistic interaction of thermal stress coupled with overstocking strongly modulates the transcriptomic activity and immune capacity of rainbow trout (Oncorhynchus mykiss). Sci. Rep. 10, 1–15 (2020).ADS 

    Google Scholar 
    Braun, N., de Lima, R. L., Baldisserotto, B., Dafre, A. L. & de Oliveira Nuñer, A. P. Growth, biochemical and physiological responses of Salminus brasiliensis with different stocking densities and handling. Aquaculture 301, 22–30 (2010).CAS 

    Google Scholar 
    Refaey, M. M., Tian, X., Tang, R. & Li, D. Changes in physiological responses, muscular composition and flesh quality of channel catfish Ictalurus punctatus suffering from transport stress. Aquaculture 478, 9–15 (2017).CAS 

    Google Scholar 
    Liu, G. et al. Influence of stocking density on growth, digestive enzyme activities, immune responses, antioxidant of Oreochromis niloticus fingerlings in biofloc systems. Fish Shellfish Immunol. 81, 416–422 (2018).CAS 
    PubMed 

    Google Scholar 
    Kumar, G. & Engle, C. R. Technological advances that led to growth of shrimp, salmon, and tilapia farming. Rev. Fish. Sci. Aquac. 24, 136–152 (2016).
    Google Scholar 
    Sundin, L. Hypoxia and blood flow control in fish gills. In Biology of tropical fishes (eds Val, A. L. & Almeida-Val, V. M. F.) 353–362 (Manaus INPA, 1999).
    Google Scholar 
    Beveridge, M. C. M. Cage Aquaculture Vol. 5 (John Wiley & Sons, 2008).
    Google Scholar 
    Valenti, W. C., Barros, H. P., Moraes-Valenti, P., Bueno, G. W. & Cavalli, R. O. Aquaculture in Brazil: past, present and future. Aquac. Rep. 19, 100611 (2021).
    Google Scholar 
    Das, A. K., Meena, D. K. & Sharma, A. P. Cage farming in an Indian Reservoir. World Aquac. 45, 56–59 (2014).
    Google Scholar 
    Sarkar, U. K. et al. Status, prospects, threats, and the way forward for sustainable management and enhancement of the tropical Indian reservoir fisheries: an overview. Rev. Fish. Sci. Aquac. 26, 155–175 (2018).
    Google Scholar 
    Singh, A. K. & Lakra, W. S. Culture of Pangasianodon hypophthalmus into India: impacts and present scenario. Pakistan J. Biol. Sci. 15, 19 (2012).CAS 

    Google Scholar 
    Jena, J. et al. Evaluation of growth performance of Labeo fimbriatus (Bloch), Labeo gonius (Hamilton) and Puntius gonionotus (Bleeker) in polyculture with Labeo rohita (Hamilton) during fingerlings rearing at varied densities. Aquaculture 319, 493–496 (2011).
    Google Scholar 
    Liu, B., Jia, R., Han, C., Huang, B. & Lei, J.-L. Effects of stocking density on antioxidant status, metabolism and immune response in juvenile turbot (Scophthalmus maximus). Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 190, 1–8 (2016).CAS 

    Google Scholar 
    Wu, F. et al. Effect of stocking density on growth performance, serum biochemical parameters, and muscle texture properties of genetically improved farm tilapia, Oreochromis niloticus. Aquac. Int. 26, 1247–1259 (2018).CAS 

    Google Scholar 
    Andrade, T. et al. Evaluation of different stocking densities in a Senegalese sole (Solea senegalensis) farm: implications for growth, humoral immune parameters and oxidative status. Aquaculture 438, 6–11 (2015).CAS 

    Google Scholar 
    Qi, C. et al. Effect of stocking density on growth, physiological responses, and body composition of juvenile blunt snout bream, Megalobrama amblycephala. J. World Aquac. Soc. 47, 358–368 (2016).CAS 

    Google Scholar 
    Shao, T. et al. Evaluation of the effects of different stocking densities on growth and stress responses of juvenile hybrid grouper♀ Epinephelus fuscoguttatus×♂ Epinephelus lanceolatus in recirculating aquaculture systems. J. Fish Biol. 95, 1022–1029 (2019).CAS 
    PubMed 

    Google Scholar 
    Adineh, H., Naderi, M., Hamidi, M. K. & Harsij, M. Biofloc technology improves growth, innate immune responses, oxidative status, and resistance to acute stress in common carp (Cyprinus carpio) under high stocking density. Fish Shellfish Immunol. 95, 440–448 (2019).CAS 
    PubMed 

    Google Scholar 
    Fazelan, Z., Vatnikov, Y. A., Kulikov, E. V., Plushikov, V. G. & Yousefi, M. Effects of dietary ginger (Zingiber officinale) administration on growth performance and stress, immunological, and antioxidant responses of common carp (Cyprinus carpio) reared under high stocking density. Aquaculture 518, 734833 (2020).CAS 

    Google Scholar 
    Hoseini, S. M., Yousefi, M., Hoseinifar, S. H. & Van Doan, H. Effects of dietary arginine supplementation on growth, biochemical, and immunological responses of common carp (Cyprinus carpio L.), stressed by stocking density. Aquaculture 503, 452–459 (2019).CAS 

    Google Scholar 
    Adineh, H., Naderi, M., Nazer, A., Yousefi, M. & Ahmadifar, E. Interactive effects of stocking density and dietary supplementation with nano selenium and garlic extract on growth, feed utilization, digestive enzymes, stress responses, and antioxidant capacity of grass carp, Ctenopharyngodon idella. J. World Aquac. Soc. 52, 789–804 (2021).CAS 

    Google Scholar 
    Zhao, H. et al. Transcriptome and physiological analysis reveal alterations in muscle metabolisms and immune responses of grass carp (Ctenopharyngodon idellus) cultured at different stocking densities. Aquaculture 503, 186–197 (2019).CAS 

    Google Scholar 
    Frisso, R. M., de Matos, F. T., Moro, G. V. & de Mattos, B. O. Stocking density of Amazon fish (Colossoma macropomum) farmed in a continental neotropical reservoir with a net cages system. Aquaculture 529, 735702 (2020).CAS 

    Google Scholar 
    Tammam, M. S., Wassef, E. A., Toutou, M. M. & El-Sayed, A.-F.M. Combined effects of surface area of periphyton substrates and stocking density on growth performance, health status, and immune response of Nile tilapia (Oreochromis niloticus) produced in cages. J. Appl. Phycol. 32, 3419–3428 (2020).CAS 

    Google Scholar 
    Zaki, M. A. A. et al. The impact of stocking density and dietary carbon sources on the growth, oxidative status and stress markers of Nile tilapia (Oreochromis niloticus) reared under biofloc conditions. Aquac. Reports 16, 100282 (2020).
    Google Scholar 
    Rowland, S. J., Mifsud, C., Nixon, M. & Boyd, P. Effects of stocking density on the performance of the Australian freshwater silver perch (Bidyanus bidyanus) in cages. Aquaculture 253, 301–308 (2006).
    Google Scholar 
    Mohler, J. W., King, M. K. & Farrell, P. R. Growth and survival of first-feeding and fingerling Atlantic sturgeon under culture conditions. N. Am. J. Aquac. 62, 174–183 (2000).
    Google Scholar 
    Mirghaed, A. T., Hoseini, S. M. & Ghelichpour, M. Effects of dietary 1, 8-cineole supplementation on physiological, immunological and antioxidant responses to crowding stress in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 81, 182–188 (2018).
    Google Scholar 
    Hoseini, S. M., Mirghaed, A. T., Iri, Y. & Ghelichpour, M. Effects of dietary cineole administration on growth performance, hematological and biochemical parameters of rainbow trout (Oncorhynchus mykiss). Aquaculture 495, 766–772 (2018).CAS 

    Google Scholar 
    Barton, B. A., Morgan, J. D. & Vijayan, M. M. Physiological and condition-related indicators of environmental stress in fish. In Biological Indicators of Aquatic Ecosystem Stress (ed. Adams, S. M.) 111–148 (American Fisheries Society, 2002).
    Google Scholar 
    Varela, J. L. et al. Dietary administration of probiotic Pdp11 promotes growth and improves stress tolerance to high stocking density in gilthead seabream Sparus auratus. Aquaculture 309, 265–271 (2010).CAS 

    Google Scholar 
    Costas, B., Aragão, C., Dias, J., Afonso, A. & Conceição, L. E. C. Interactive effects of a high-quality protein diet and high stocking density on the stress response and some innate immune parameters of Senegalese sole Solea senegalensis. Fish Physiol. Biochem. 39, 1141–1151 (2013).CAS 
    PubMed 

    Google Scholar 
    Long, L. et al. Effects of stocking density on growth, stress, and immune responses of juvenile Chinese sturgeon (Acipenser sinensis) in a recirculating aquaculture system. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 219, 25–34 (2019).CAS 

    Google Scholar 
    Sadhu, N., Sharma, S. R. K., Joseph, S., Dube, P. & Philipose, K. K. Chronic stress due to high stocking density in open sea cage farming induces variation in biochemical and immunological functions in Asian seabass (Lates calcarifer, Bloch). Fish Physiol. Biochem. 40, 1105–1113 (2014).CAS 
    PubMed 

    Google Scholar 
    Zahran, E., Risha, E., AbdelHamid, F., Mahgoub, H. A. & Ibrahim, T. Effects of dietary Astragalus polysaccharides (APS) on growth performance, immunological parameters, digestive enzymes, and intestinal morphology of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol. 38, 149–157 (2014).CAS 
    PubMed 

    Google Scholar 
    Aruoma, O. I. Free radicals, oxidative stress, and antioxidants in human health and disease. J. Am. Oil Chem. Soc. 75, 199–212 (1998).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Haridas, H. et al. Enhanced growth and immuno-physiological response of genetically improved farmed Tilapia in indoor biofloc units at different stocking densities. Aquac. Res. 48, 4346–4355 (2017).CAS 

    Google Scholar 
    Ruane, N. M., Carballo, E. C. & Komen, J. Increased stocking density influences the acute physiological stress response of common carp Cyprinus carpio (L.). Aquac. Res. 33, 777–784 (2002).
    Google Scholar 
    Wang, X. et al. Effects of stocking density on growth, nonspecific immune response, and antioxidant status in African catfish (Clarias gariepinus). (2013).Johnson, K. M. & Lema, S. C. Tissue-specific thyroid hormone regulation of gene transcripts encoding iodothyronine deiodinases and thyroid hormone receptors in striped parrotfish (Scarus iseri). Gen. Comp. Endocrinol. 172, 505–517 (2011).CAS 
    PubMed 

    Google Scholar 
    El-Khaldi, A. T. F. Effect of different stress factors on some physiological parameters of Nile tilapia (Oreochromis niloticus). Saudi J. Biol. Sci. 17, 241–246 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sharma, A., Devi, S., Singh, K. & Prabhakar, P. K. Correlation of body mass index with thyroid-stimulating hormones in thyroid patient. Asian J. Pharm. Clin. Res. 11, 65–68 (2018).
    Google Scholar 
    Li, D., Liu, Z. & Xie, C. Effect of stocking density on growth and serum concentrations of thyroid hormones and cortisol in Amur sturgeon, Acipenser schrenckii. Fish Physiol. Biochem. 38, 511–520 (2012).CAS 
    PubMed 

    Google Scholar 
    Park, J.-W. et al. The thyroid endocrine disruptor perchlorate affects reproduction, growth, and survival of mosquitofish. Ecotoxicol. Environ. Saf. 63, 343–352 (2006).CAS 
    PubMed 

    Google Scholar 
    Refaey, M. M. et al. High stocking density alters growth performance, blood biochemistry, intestinal histology, and muscle quality of channel catfish Ictalurus punctatus. Aquaculture 492, 73–81 (2018).CAS 

    Google Scholar 
    Reinecke, M. et al. Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen. Comp. Endocrinol. 142, 20–24 (2005).CAS 
    PubMed 

    Google Scholar 
    Salas-Leiton, E. et al. Dexamethasone modulates expression of genes involved in the innate immune system, growth and stress and increases susceptibility to bacterial disease in Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol. 32, 769–778 (2012).CAS 
    PubMed 

    Google Scholar 
    Dyer, A. R. et al. Correlation of plasma IGF-I concentrations and growth rate in aquacultured finfish: a tool for assessing the potential of new diets. Aquaculture 236, 583–592 (2004).CAS 

    Google Scholar 
    Kajimura, S. et al. Dual mode of cortisol action on GH/IGF-I/IGF binding proteins in the tilapia, Oreochromis mossambicus. J. Endocrinol. 178, 91–99 (2003).CAS 
    PubMed 

    Google Scholar 
    Ren, Y., Wen, H., Li, Y. & Li, J. Stocking density affects the growth performance and metabolism of Amur sturgeon by regulating expression of genes in the GH/IGF axis. J. Oceanol. Limnol. 36, 956–972 (2018).ADS 
    CAS 

    Google Scholar 
    Salas-Leiton, E. et al. Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Fish Shellfish Immunol. 28, 296–302 (2010).CAS 
    PubMed 

    Google Scholar 
    Vijayan, M. M., Aluru, N. & Leatherland, J. F. Stress response and the role of cortisol. Fish Dis. Disord. 2, 182–201 (2010).
    Google Scholar 
    Hegazi, M. M., Attia, Z. I. & Ashour, O. A. Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat. Toxicol. 99, 118–125 (2010).CAS 
    PubMed 

    Google Scholar 
    Kpundeh, M. D., Xu, P., Yang, H., Qiang, J. & He, J. Stocking densities and chronic zero culture water exchange stress’ effects on biological performances, hematological and serum biochemical indices of GIFT tilapia juveniles (Oreochromis niloticus). J. Aquac. Res. Dev. 4, 2 (2013).
    Google Scholar 
    Tan, C. et al. Effects of stocking density on growth, body composition, digestive enzyme levels and blood biochemical parameters of Anguilla marmorata in a recirculating aquaculture system. Turk. J. Fish. Aquat. Sci. 18, 9–16 (2018).
    Google Scholar 
    Ni, M. et al. The physiological performance and immune responses of juvenile Amur sturgeon (Acipenser schrenckii) to stocking density and hypoxia stress. Fish Shellfish Immunol. 36, 325–335 (2014).CAS 
    PubMed 

    Google Scholar 
    Abdel-Tawwab, M. Effects of dietary protein levels and rearing density on growth performance and stress response of Nile tilapia, Oreochromis niloticus (L.). Int. Aquat. Res. 4, 1–13 (2012).
    Google Scholar 
    Chatterjee, N. et al. Effect of stocking density and journey length on the welfare of rohu (Labeo rohita Hamilton) fry. Aquac. Int. 18, 859–868 (2010).
    Google Scholar 
    Pakhira, C., Nagesh, T. S., Abraham, T. J., Dash, G. & Behera, S. Stress responses in rohu, Labeo rohita transported at different densities. Aquac. Rep. 2, 39–45 (2015).
    Google Scholar 
    Tahmasebi-Kohyani, A., Keyvanshokooh, S., Nematollahi, A., Mahmoudi, N. & Pasha-Zanoosi, H. Effects of dietary nucleotides supplementation on rainbow trout (Oncorhynchus mykiss) performance and acute stress response. Fish Physiol. Biochem. 38, 431–440 (2012).CAS 
    PubMed 

    Google Scholar 
    Montero, D. et al. Effect of vitamin E and C dietary supplementation on some immune parameters of gilthead seabream (Sparus aurata) juveniles subjected to crowding stress. Aquaculture 171, 269–278 (1999).CAS 

    Google Scholar 
    Urbinati, E. C., de Abreu, J. S., da Silva Camargo, A. C. & Parra, M. A. L. Loading and transport stress of juvenile matrinxã (Brycon cephalus, Characidae) at various densities. Aquaculture 229, 389–400 (2004).
    Google Scholar 
    Evans, D. H. Cell signaling and ion transport across the fish gill epithelium. J. Exp. Zool. 293, 336–347 (2002).CAS 
    PubMed 

    Google Scholar 
    McCormick, S. D. Endocrine control of osmoregulation in teleost fish. Am. Zool. 41, 781–794 (2001).CAS 

    Google Scholar 
    Postlethwaite, E. & McDonald, D. Mechanisms of Na+ and C-regulation in freshwater-adapted rainbow trout (Oncorhynchus mykiss) during exercise and stress. J. Exp. Biol. 198, 295–304 (1995).CAS 
    PubMed 

    Google Scholar 
    Liu, P., Du, Y., Meng, L., Li, X. & Liu, Y. Metabolic profiling in kidneys of Atlantic salmon infected with Aeromonas salmonicida based on 1H NMR. Fish Shellfish Immunol. 58, 292–301 (2016).CAS 
    PubMed 

    Google Scholar 
    Hosfeld, C. D., Hammer, J., Handeland, S. O., Fivelstad, S. & Stefansson, S. O. Effects of fish density on growth and smoltification in intensive production of Atlantic salmon (Salmo salar L.). Aquaculture 294, 236–241 (2009).
    Google Scholar 
    Wagner, E. I., Miller, S. A. & Bosakowski, T. Ammonia excretion by rainbow trout over a 24-hour period at two densities during oxygen injection. Progress. Fish-Culturist 57, 199–205 (1995).
    Google Scholar 
    Dong, J. et al. Effect of stocking density on growth performance, digestive enzyme activities, and nonspecific immune parameters of Palaemonetes sinensis. Fish Shellfish Immunol. 73, 37–41 (2018).CAS 
    PubMed 

    Google Scholar 
    Wang, Y. et al. Effects of stocking density on the growth performance, digestive enzyme activities, antioxidant resistance, and intestinal microflora of blunt snout bream (Megalobrama amblycephala) juveniles. Aquac. Res. 50, 236–246 (2019).CAS 

    Google Scholar 
    Trenzado, C. E. et al. Effect of dietary lipid content and stocking density on digestive enzymes profile and intestinal histology of rainbow trout (Oncorhynchus mykiss). Aquaculture 497, 10–16 (2018).CAS 

    Google Scholar 
    Li, X., Liu, Y. & Blancheton, J.-P. Effect of stocking density on performances of juvenile turbot (Scophthalmus maximus) in recirculating aquaculture systems. Chin. J. Oceanol. Limnol. 31, 514–522 (2013).ADS 
    CAS 

    Google Scholar 
    Ezhilmathi, S. et al. Effect of stocking density on growth performance, digestive enzyme activity, body composition and gene expression of Asian seabass reared in recirculating aquaculture system. Aquac. Res. https://doi.org/10.1111/are.15725 (2022).Article 

    Google Scholar 
    Bolasina, S., Tagawa, M., Yamashita, Y. & Tanaka, M. Effect of stocking density on growth, digestive enzyme activity and cortisol level in larvae and juveniles of Japanese flounder, Paralichthys olivaceus. Aquaculture 259, 432–443 (2006).CAS 

    Google Scholar 
    Hoseini, S. M., Hoseinifar, S. H. & Van Doan, H. Effect of dietary eucalyptol on stress markers, enzyme activities and immune indicators in serum and haematological characteristics of common carp (Cyprinus carpio) exposed to toxic concentration of ambient copper. Aquac. Res. 49, 3045–3054 (2018).CAS 

    Google Scholar 
    Ni, M. et al. Effects of stocking density on mortality, growth and physiology of juvenile Amur sturgeon (Acipenser schrenckii). Aquac. Res. 47, 1596–1604 (2016).CAS 

    Google Scholar 
    Abdel-Tawwab, M., Hagras, A. E., Elbaghdady, H. A. M. & Monier, M. N. Dissolved oxygen level and stocking density effects on growth, feed utilization, physiology, and innate immunity of Nile Tilapia, Oreochromis niloticus. J. Appl. Aquac. 26, 340–355 (2014).
    Google Scholar 
    Toko, I., Fiogbe, E. D., Koukpode, B. & Kestemont, P. Rearing of African catfish (Clarias gariepinus) and vundu catfish (Heterobranchus longifilis) in traditional fish ponds (whedos): effect of stocking density on growth, production and body composition. Aquaculture 262, 65–72 (2007).
    Google Scholar 
    Suárez, M. D. et al. Influence of dietary lipids and culture density on rainbow trout (Oncorhynchus mykiss) flesh composition and quality parameter. Aquac. Eng. 63, 16–24 (2014).
    Google Scholar 
    Santín, A., Grinyó, J., Bilan, M., Ambroso, S. & Puig, P. First report of the carnivorous sponge Lycopodina hypogea (Cladorhizidae) associated with marine debris, and its possible implications on deep-sea connectivity. Mar. Pollut. Bull. 159, 111501 (2020).PubMed 

    Google Scholar 
    Jørpeland, G., Imsland, A., Stien, L. H., Bleie, H. & Roth, B. Effects of filleting method, stress, storage and season on the quality of farmed Atlantic cod (Gadus morhua L.). Aquac. Res. 46, 1597–1607 (2015).
    Google Scholar 
    Bulow, F. J. RNA-DNA ratios as indicators of growth in fish: a review. In The Age and growth of fish (eds Summerfelt, R. C. & Hall, G. E.) 45–64 (Iowa State University Press, Ames, Iowa, 1987).
    Google Scholar 
    Regnault, M. & Luquet, P. Study by evolution of nucleic acid content of prepuberal growth in the shrimp Crangon vulgaris. Mar. Biol. 25, 291–298 (1974).CAS 

    Google Scholar 
    Tanaka, H. K. M. et al. High resolution imaging in the inhomogeneous crust with cosmic-ray muon radiography: the density structure below the volcanic crater floor of Mt. Asama, Japan. Earth Planet. Sci. Lett. 263, 104–113 (2007).ADS 
    CAS 

    Google Scholar 
    Gwak, W. S. & Tanaka, M. Developmental change in RNA: DNA ratios of fed and starved laboratory-reared Japanese flounder larvae and juveniles, and its application to assessment of nutritional condition for wild fish. J. Fish Biol. 59, 902–915 (2001).CAS 

    Google Scholar 
    Ali, M., Iqbal, R., Rana, S. A., Athar, M. & Iqbal, F. Effect of feed cycling on specific growth rate, condition factor and RNA/DNA ratio of Labeo rohita. African J. Biotechnol. 5, 1551–1556 (2006).CAS 

    Google Scholar 
    Zehra, S. & Khan, M. A. Dietary lysine requirement of fingerling Catla catla (Hamilton) based on growth, protein deposition, lysine retention efficiency, RNA/DNA ratio and carcass composition. Fish Physiol. Biochem. 39, 503–512 (2013).CAS 
    PubMed 

    Google Scholar 
    Misra, H. P. & Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247, 3170–3175 (1972).CAS 
    PubMed 

    Google Scholar 
    Takahara, S. et al. Hypocatalasemia: a new genetic carrier state. J. Clin. Invest. 39, 610–619 (1960).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rick, W. & Stegbauer, H. P. α-Amylase measurement of reducing groups. In Methods of Enzymatic Analysis (ed. Bergmeyer, H. S.) 885–890 (Elsevier, 1974).
    Google Scholar 
    Cherry, I. S. & Crandall, L. A. Jr. The specificity of pancreatic lipase: its appearance in the blood after pancreatic injury. Am. J. Physiol. Content 100, 266–273 (1932).CAS 

    Google Scholar 
    Drapeau, G. R. [38] Protease from Staphyloccus aureus. In Methods in Enzymology (eds Jura, N. & Murphy, J. M.) 469–475 (Elsevier, 1976).
    Google Scholar 
    AOAC. Official Methods of Analysis of AOAC International. (Association of Official Analytical Chemists Washington, DC, 2005).Bosworth, B. G., Small, B. C. & Mischke, C. Effects of transport water temperature, aerator type, and oxygen level on channel catfish Ictalurus punctatus fillet quality. J. World Aquac. Soc. 35, 412–419 (2004).
    Google Scholar 
    Ma, L. Q., Qi, C. L., Cao, J. J. & Li, D. P. Comparative study on muscle texture profile and nutritional value of channel catfish (Ictalurus punctatus) reared in ponds and reservoir cages. J. Fish. China 38, 532–537 (2014).
    Google Scholar 
    APHA. Standard Methods for the Examination of Water and Wastewater. (American Public Health Association, American Water Works Association, Water Environment Federation, 2012). More