More stories

  • in

    Community context matters for bacteria-phage ecology and evolution

    1.Crick FHC, Barnett FRSL, Brenner S, Watts-Tobin RJ. General Nature of the Genetic Code for Proteins. Nature. 1961;192:1227–32.CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Hershey AD, Chase M. Independent functions of viral protein and nucleic acid in growth of bacteriophage. J Gen Physiol. 1952;36:39–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Luria S, Delbrück M. Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics. 1943;28:491–511.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Kortright KE, Chan BK, Koff JL, Turner PE. Phage Therapy: a Renewed Approach to Combat Antibiotic-Resistant Bacteria. Cell Host Microbe. 2019;25:219–32.CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Mushegian AR. Are there 10^31 virus particles on Earth, or more, or less? J Bacteriol. 2020;202:e00052–20.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Dennehy JJ. What Can Phages Tell Us about Host-Pathogen Coevolution? Int J Evol Biol. 2012;2012:1–12.Article 

    Google Scholar 
    7.Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, et al. Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol. 2004;19:189–97.PubMed 
    Article 

    Google Scholar 
    8.Tecon R, Mitri S, Ciccarese D, Or D, Meer JR, van der, Johnson DR. Bridging the Holistic-Reductionist Divide in Microbial Ecology. MSystems. 2019;4:e00265–18.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Bohannan BJM, Lenski RE. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett. 2000;3:362–77.Article 

    Google Scholar 
    10.Buckling A, Brockhurst MA. Bacteria-Virus Coevolution. In: Orkun S Soyer, editor. Evolutionary Systems Biology. 2012. New York, NY: Springer; 2012. p. 347–70.11.Koskella B, Brockhurst MA. Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev. 2014;38:1–16.Article 
    CAS 

    Google Scholar 
    12.De Sordi L, Lourenço M, Debarbieux L. The Battle Within: interactions of Bacteriophages and Bacteria in the Gastrointestinal Tract. Cell Host Microbe. 2019;25:210–8.PubMed 
    Article 
    CAS 

    Google Scholar 
    13.Scanlan PD. Bacteria–Bacteriophage Coevolution in the Human Gut: implications for Microbial Diversity and Functionality. Trends Microbiol. 2017;25:614–23.CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Breitbart M. Marine viruses: truth or dare. Annu Rev Mar Sci. 2012;4:425–48.Article 

    Google Scholar 
    15.Pratama AA, van Elsas JD. The ‘neglected’ soil virome–potential role and impact. Trends Microbiol. 2018;26:649–62.CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Lourenço M, De Sordi L, Debarbieux L. The diversity of bacterial lifestyles hampers bacteriophage tenacity. Viruses. 2018;10:1–11.Article 
    CAS 

    Google Scholar 
    17.Martiny JBH, Riemann L, Marston MF, Middelboe M. Antagonistic Coevolution of Marine Planktonic Viruses and Their Hosts. Annu Rev Mar Sci. 2014;6:393–414.Article 

    Google Scholar 
    18.Díaz-Muñoz SL, Koskella B. Bacteria–Phage Interactions in Natural Environments. In: Sariaslani S, Gadd GM, editors. Advances in Applied Microbiology. Cambridge, MA:Academic Press; 2014. p.135–83.19.Avrani S, Schwartz DA, Lindell D. Virus-host swinging party in the oceans. Mob Genet Elem. 2012;2:88–95.Article 

    Google Scholar 
    20.Winter C, Bouvier T, Weinbauer MG, Thingstad TF. Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited. Microbiol Mol Biol Rev. 2010;74:42–57.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Hansen MF, Svenningsen SL, Røder HL, Middelboe M, Burmølle M. Big Impact of the Tiny: bacteriophage–bacteria Interactions in Biofilms. Trends Microbiol. 2019;27:739–52.CAS 
    PubMed 
    Article 

    Google Scholar 
    22.O’Brien S, Hodgson DJ, Buckling A. The interplay between microevolution and community structure in microbial populations. Curr Opin Biotechnol. 2013;24:821–5.PubMed 
    Article 
    CAS 

    Google Scholar 
    23.Brockhurst MA, Koskella B. Experimental coevolution of species interactions. Trends Ecol Evol. 2013;28:367–75.PubMed 
    Article 

    Google Scholar 
    24.Geredew Kifelew L, Mitchell JG, Speck P. Mini-review: efficacy of lytic bacteriophages on multispecies biofilms. Biofouling. 2019;35:472–81.CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Miki T, Jacquet S. Complex interactions in the microbial world: Underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat Micro Ecol. 2008;51:195–208.Article 

    Google Scholar 
    26.Johnke J, Cohen Y, de Leeuw M, Kushmaro A, Jurkevitch E, Chatzinotas A. Multiple micro-predators controlling bacterial communities in the environment. Curr Opin Biotechnol. 2014;27:185–90.CAS 
    PubMed 
    Article 

    Google Scholar 
    27.Hall AR, Ashby B, Bascompte J, King KC. Measuring Coevolutionary Dynamics in Species-Rich Communities. Trends Ecol Evol. 2020;35:539–50.PubMed 
    Article 

    Google Scholar 
    28.Strauss SY. Ecological and evolutionary responses in complex communities: implications for invasions and eco-evolutionary feedbacks. Oikos. 2014;123:257–66.Article 

    Google Scholar 
    29.Strauss SY, Irwin RE. Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst. 2004;35:435–66.Article 

    Google Scholar 
    30.Inouye B, Stinchcombe JR. Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links. Oikos. 2011;95:353–60.Article 

    Google Scholar 
    31.Barraclough TG. How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities? Annu Rev Ecol Evol Syst. 2015;46:25–48.Article 

    Google Scholar 
    32.Bottery MJ, Pitchford JW, Friman V-P. Ecology and evolution of antimicrobial resistance in bacterial communities. ISME J. 2021;15:939–48.PubMed 
    Article 

    Google Scholar 
    33.Gómez P, Bennie J, Gaston KJ, Buckling A. The Impact of Resource Availability on Bacterial Resistance to Phages in Soil. PLoS ONE. 2015;10:e0123752.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Gorter FA, Scanlan PD, Buckling A. Adaptation to abiotic conditions drives local adaptation in bacteria and viruses coevolving in heterogeneous environments. Biol Lett. 2016;12:20150879.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    35.Scanlan JG, Hall AR, Scanlan PD. Impact of bile salts on coevolutionary dynamics between the gut bacterium Escherichia coli and its lytic phage PP01. Infect Genet Evol. 2019;73:425–32.CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Gómez P, Buckling A. Bacteria-phage antagonistic coevolution in soil. Science. 2011;332:106–9.PubMed 
    Article 
    CAS 

    Google Scholar 
    37.Weinbauer MG, Rassoulzadegan F. Are viruses driving microbial diversification and diversity? Environ Microbiol. 2004;6:1–11.PubMed 
    Article 

    Google Scholar 
    38.Johnke J, Baron M, de Leeuw M, Kushmaro A, Jurkevitch E, Harms H, et al. A generalist protist predator enables coexistence in multitrophic predator-prey systems containing a phage and the bacterial predator Bdellovibrio. Front Ecol Evol. 2017;5:1–12.Article 

    Google Scholar 
    39.R Core Team. R: a Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2020.40.Mumford R, Friman VP. Bacterial competition and quorum-sensing signalling shape the eco-evolutionary outcomes of model in vitro phage therapy. Evol Appl. 2017;10:161–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Connell JH. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology. 1961;42:710–23.Article 

    Google Scholar 
    42.Vellend M. Conceptual Synthesis in Community Ecology. Q Rev Biol. 2010;85:183–206.PubMed 
    Article 

    Google Scholar 
    43.Alseth EO, Pursey E, Lujan AM, McLeod I, Rollie C, Westra ER. Bacterial biodiversity drives the evolution of CRISPR-based phage resistance in Pseudomonas aeruginosa. Nature. 2019;574:549–74.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Goldhill DH, Turner PE. The evolution of life history trade-offs in viruses. Curr Opin Virol. 2014;8:79–84.PubMed 
    Article 

    Google Scholar 
    45.Keen EC. Tradeoffs in bacteriophage life histories. Bacteriophage. 2014;4:e28365.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Gómez P, Buckling A. Real-time microbial adaptive diversification in soil. Ecol Lett. 2013;16:650–5.PubMed 
    Article 

    Google Scholar 
    47.Houte S, van, Buckling A, Westra ER. Evolutionary Ecology of Prokaryotic Immune Mechanisms. Microbiol Mol Biol Rev. 2016;80:745–63.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Middelboe M, Hagström A, Blackburn N, Sinn B, Fischer U, Borch NH, et al. Effects of bacteriophages on the population dynamics of four strains of pelagic marine bacteria. Micro Ecol. 2001;42:395–406.CAS 
    Article 

    Google Scholar 
    49.Gómez P, Buckling A. Coevolution with phages does not influence the evolution of bacterial mutation rates in soil. ISME J. 2013;7:2242–4.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    50.De Sordi L, Khanna V, Debarbieux L. The Gut Microbiota Facilitates Drifts in the Genetic Diversity and Infectivity of Bacterial Viruses. Cell Host Microbe. 2017;22:801–8.e3.CAS 
    PubMed 
    Article 

    Google Scholar 
    51.De Sordi L, Lourenço M, Debarbieux L. “I will survive”: A tale of bacteriophage-bacteria coevolution in the gut. Gut Microbes. 2019;10:92–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Landsberger M, Gandon S, Meaden S, Chabas H, Buckling A, Westra ER, et al. Anti-CRISPR phages cooperate to overcome CRISPR-Cas immunity. Cell. 2018;174:908–16.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Westra ER, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM, Best A, et al. Parasite exposure drives selective evolution of constitutive versus inducible defense. Curr Biol. 2015;25:1043–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Dy RL, Richter C, Salmond GP, Fineran PC. Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol. 2014;1:307–31.PubMed 
    Article 
    CAS 

    Google Scholar 
    55.Rostøl JT, Marraffini L. (Ph)ighting phages: how bacteria resist their parasites. Cell Host Microbe. 2019;25:184–94.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    56.Burmeister AR, Turner PE. Trading-off and trading-up in the world of bacteria–phage evolution. Curr Biol. 2020;30:R1120–R1124.CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Plummer M. JAGS: a program for analysis of Bayesian graphical models using Gibbs sampling. Vienna, Austria: Proc. 3rd Int. Workshop Distrib. Stat. Comput; 2003. p. 1–10.58.Wickham H. ggplot2: elegant Graphics for Data Analysis. Verlag New York: Springer; 2016.59.Wickham H. tidyr: Tidy Messy Data. 2020.60.Plummer M. rjags: Bayesian Graphical Models using MCMC. 2019.61.Wickham H, François R, Henry L, Müller K. dplyr: A Grammar of Data Manipulation. 2020.62.Gandon S, Buckling A, Decaestecker E, Day T. Host-parasite coevolution and patterns of adaptation across time and space. J Evol Biol. 2008;21:1861–6.CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Publisher Correction: Reflections and projections on a decade of climate science

    Deutsches Zentrum für Luft- und Raumfahrt e.V. (DLR), Institut für Physik der Atmosphäre, Oberpfaffenhofen, GermanyVeronika EyringInstitute of Environmental Physics (IUP), University of Bremen, Bremen, GermanyVeronika EyringCivil Engineering and Earth Sciences, Indian Institute of Technology (IIT) Gandhinagar, Gandhinagar, IndiaVimal MishraNorwegian Polar Institute, FRAM – High North Research Centre on Climate and the Environment, Tromsø, NorwayGary P. GriffithLevin Lab, Ecology & Evolutionary Biology, Princeton University, Princeton, NJ, USAGary P. GriffithKey Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, ChinaLei ChenDepartment of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA, USATrevor KeenanEcology and Evolutionary Biology Department, University of Colorado, Boulder, CO, USAMerritt R. TuretskyDepartment of Life and Environmental Sciences, Bournemouth University, Poole, UKSally BrownAustralian National University, Crawford School of Public Policy, Canberra, Australian Capital Territory, AustraliaFrank JotzoEnvironmental Science and Policy, University of California, Davis, Davis, CA, USAFrances C. MooreDepartment of Psychology, School of Biological Sciences, University of Cambridge, Cambridge, UKSander van der Linden More

  • in

    Integrating spatial analysis and questionnaire survey to better understand human-onager conflict in Southern Iran

    Study areaQatruiyeh National Park, established in 2008, is a core zone in the Bahram-e-Goor Protected Area (established in 1972) at the border of Fars and Kerman provinces in southern Iran (Fig. 1). It covers 310 km2 and is part of the Zagros Mountains. It is a semi-desert with temperate arid climate, vegetated mainly with Zygophyllum eurypterum and Artemisia sieberi20. There are seven villages in the vicinity of the protected area, where pastoralism is the main source of livelihood21.Figure 1Location of the study area. The software ArcGIS. Version 10.2. was used to generate figure. DEM map was downloaded from the WorldClim database (http://www.worldclim.org).Full size imageOne of the major threats for the Persian onager populations in this area is increasing construction of new roads and increasing road traffic. The Sirjan-Yazd (Hassan Abad-Meshkaan) asphalt road, which passes through the Bahram-e-Goor Protected Area, was recently converted into a highway and represents a substantial threat to Onagers (Fig. 1). This road has two lanes in each direction. The day-time speed limit on this road is 110 km/h and 90 km/h at night. Most vehicles on this road are heavy trucks, which pass at high speed (more than 90 km/h), with high traffic volumes at night. During winter, late autumn and summer of drought years, when fodder is scarce, onagers frequently cross the road to access gardens and agricultural fields, which causes high onager mortality due to vehicle collisions. In this research, we used spatial randomization of vehicle collisions and crossing locations to test the predictive ability of resistant kernel and factorial least-cost path predictions of movement18. We also conducted questionnaires with residents from local communities to determine the most important factors influencing human-onager conflicts in the Bahram-e-Goor Protected Area.Human-onager conflict assessmentQualitative data collectionWe administered a questionnaire through a personal interview to 200 randomly chosen farmers residing near onager populations in the Bahram-e-Goor Protected Area in Fars province. Data were collected through a questionnaire between May and August 2018 (Table S1). Ethical clearance was obtained from the DOE (under permit 32–239). All participants were given a printed descriptive summary of the research (if participants were illiterate, the document was read to them). Prior informed consent was obtained orally from all participants. In this research, we followed legal requirements of ethical issues.We calculated the sample size needed by using the family size in rural areas around Bahram-e-Goor Protected Area using the Daniel method22 (Table S1) as described below (Eq. 1):We randomly conducted 200 questionnaires in total.$$N=frac{ {Z}^{2 }P (1-P) }{{d}^{2}}$$
    (1)
    In this equation, Z is the Z statistic for a level of confidence, P is expected prevalence or proportion (if the expected prevalence is 20%, then P = 0.2), and d is precision (if the precision is 5%, then d = 0.05). In this research, we used d = 0.5 and p was selected according to family sizes in each district of rural areas22.All interviewees were adult males. We collected information on interviewees’ demographic and socioeconomic background (occupation, property, age, and income) as well as their knowledge and opinion on how to prevent onager crop-raiding.We used logistic regression to analyze the significance of sociological factors related to crop damage by onagers. Our dependent variable was “Have you had any of your crop raided by onager during the last year? (Binary response: 1 = Yes, 0 = No)”. Our independent variables included: (1) traditional solutions for reducing Persian onager damages (Response: 1 guarding dogs, 2: fencing around agricultural land, 3: use of traditional barriers (a plastic cuff with a bell on it), 4: scarecrow, 5: turn on the lights at night , 6: Bird-Scarer (Kalaghparan in Persian); (2) which of these solutions could be effective in reducing Persian onager damages (Responses included: 1: fencing around Persian onager habitat, 2: fencing around farmland, 3: give fodder and provide water for Persian onager, 4: buying fodder from local people by DoE, 4: capturing and relocating Persian onager); (3): do you agree with Persian onager hunting? (Binary response: 1 = Yes, 0= No); (4): what is the role of the Persian onager in the wild? (Response 1: distributing seed of plants, the rangelands are restored, 2: it attracts tourists in the region, 3: beauty of nature: God’s creature with a right to live (Intrinsic value), 4: none) (5): age (response: 1:  50 Years), (6): education (response: 1: Incomplete Elementary (lower than 5th grade of elementary), 2: Complete Elementary (5th grade of elementary), 3: Incomplete High school, 4: Associate Degree, 5: Bachelor of Science (BSc), 5: Master of Science (MSc) or Higher), (7) Experience of Persian onager observation in nature: Have you ever seen a Persian onager in the wild? (Response scale: 1 = Yes, frequently, 2 = Yes, several times, 3: Yes, a few times 4: No, never, 5: only seen the Asiatic wild ass carcass), (8) the presence of a Persian onager around your village damages your farms and gardens. How do you feel about this statement? (Response scale) 1: completely disagree, 2: Somewhat disagree, 3: I do not agree or disagree, 4: I agree somewhat, 5: completely agree.All statistical tests were conducted in IBM SPSS Statistics (V. 23.0). Independent variables in the logistic regression analysis were coded as showed in Table S1.Naïve Bayes classificationNaïve Bayes Classification uses a group of simple classifiers based on probabilities, which are applicable to the types of random independent variables in our study. This approach is a supervised machine learning algorithm based on the Bayes Theorem that is used to solve classification problems by following a probabilistic approach. We used the e1071 library23 in R version 3.5.324 for Naïve Bayes classification of onager crop-raiding under this scheme. We considered: Yes (local communities with experience of crop-raid damages), or No (local communities without experience of crop-raid damages during the last one year) as a dependent variable, as a function of the independent variables described in logistic regression section, except we also included farm land area (1:  5 ha) as an additional variable.We categorized data into two groups (testing and training) to determine whether the model performed correctly based on training data. Subsequently, 70% of the data were used to test and run the model along with training confirmation. The Naïve Bayes Classifier was trained to anticipate each attitude in the test data. We calculated the randomness of our results using the Mclust library25 in R version 3.5.324.Onager vehicle collisionsA 25-km section of the 99-km Hassan Abad-Meshkaan road (the area with the highest wildlife-vehicle collision reports) was monitored by motorcycling and walking daily from August to October 2017 (3 weeks). Every morning, we inspected for mammal roadkill within a 30-m buffer on each side of the road, and all carcasses of mammals were recorded using a handheld GPS (Garmin GPS Map 62S). To avoid double-counting, we removed the carcasses after recording. We also obtained collision location data during 2004–2018 from the DoE.The crossing data for onager were obtained from a variety of sources including opportunistic direct observation, environmental guard’s information, and monitoring by LED portable flashlight at night (summer and autumn seasons of 2017 and 2018).Habitat connectivity analysisHabitat suitability modelingA total of 103 presence points were obtained from DoE (2015) in the study area, including Bahram-e-Goor Protected Area, as well as nearby surroundings. To minimize spatial autocorrelation, a 1-km radius was used to eliminate points around each presence location using the SDM toolbox26. The remaining 90 presence points were used in the modeling.A habitat suitability map for onager was developed using MaxEnt software version 3.3.3k27 to create a resistance map for connectivity modeling28. We used 10,000 pseudo-absence points29. For the training data set, 75% of the presence points were randomly chosen to train and the remaining 25% were used to test the model30. We used the area under the ROC curve (AUC) to evaluate model performance. MaxEnt models were completed with 10 bootstrapped replicates.Environmental layers included in MaxEnt modeling included (1) elevation (digital elevation model [DEM]), (2) slope, (3) land cover, (4) distance from agricultural lands, (5) distance from roads and (6) distance from villages. All layers had a 30 m × 30 m resolution (Table 1).Table 1 Environmental variables used for habitat modeling of the Persian onager in the study area.Full size tableSlope was calculated from the DEM layer. Land cover for 27 vegetation classes in the study area was reclassified to 10 classes based on similarities between classes in the original landcover map and due to the importance of agricultural lands (5% of the study area) to onagers. Distance from agricultural lands, roads and villages were included as predictor variables, and were calculated with the Euclidean distance tool in the Spatial Analyst extension of ArcGIS 10.2. We checked for multi-collinearity among variables and correlation was  3 were used as a threshold to exclude variables32. VIF ranged from 1.2 to 1.8 for all variables. Therefore, all variables were retained for habitat modeling.Resistance surface for connectivity analysisTo estimate landscape resistance, we converted the habitat suitability maps to resistance maps using a negative exponential function (R = 1000(−1×HS)) where R represents the cost resistance value assigned to each pixel and HS represents the predicted habitat suitability derived from the suitability models described above33. We used 1000 as the base of our exponential decay function such that areas with  > 0.3 habitat suitability would have low-cost resistance. We rescaled the resistance values to a range between 1 and 100 by linear interpolation, such that minimum resistance (Rmin) was 1 when HS was 1, and maximum resistance (Rmax) was 100 when HS was 033.Connectivity corridor network simulationWe used the universal corridor network simulator (UNICOR)34 to predict movement core areas and corridors for Onagers. UNICOR’s key features include a driver-module framework, connectivity mapping with thresholding and buffering, and graph theory metrics. UNICOR produces two kinds of connectivity predictions: (1) resistant kernels16 and (2) factorial least-cost paths15. The factorial least-cost path analysis implanted in UNICOR simulator uses Dijkstra’s algorithm34 to solve the single-source shortest path problem from every mapped species occurrence location on a landscape to every other occurrence location34. The analysis produces predicted least-cost path routes from each source point to each destination point. The resistant kernel algorithm calculates the resistance cost weighted dispersal kernel around each source point up to a user-defined dispersal threshold, and then sums these, producing an incidence function of the rate of organism movement through every pixel in the landscape as a function of the number and density of source points, the dispersal ability of the species, and the resistance of the landscape.According to observation and reports of experts in the DoE, the maximum dispersal of threshold for movement of Onagers is about 100 km. We thus specified a dispersal threshold of 100,000 cost units for the resistant kernel analysis35. We calculated the factorial least-cost path network without dispersal the threshold35 to provide a broad-scale assessment of the regional pattern of potential linkage and to map corridors. The buffered least-cost paths were then combined through summation15 to produce maps of connectivity among all pairs of presence points.Evaluating congruence between crossing points and predicted connectivityWe used a spatial randomization testing procedure to evaluate congruence between the locations where onagers were observed crossing the road and resistant kernel values of predicted connectivity18. Spatial randomization testing of this kind is recommended in cases where there is spatial dependence among observations, and produces an unbiased estimate of the probability of the observed outcome given the data18.We compared the median value of predicted connectivity (resistant kernel) for the 104 actual onager crossing locations with the distribution of median values of 1 × 107 random samples of 104 locations along the highway within the study area. For each combination of resistance surface and connectivity modeling approach, we calculated the ranking of the median of observed values within the distribution of the medians of the 1 × 107 random samples. More

  • in

    Major ocean currents may shape the microbiome of the topshell Phorcus sauciatus in the NE Atlantic Ocean

    1.Rees, H. C. et al. The detection of aquatic animal species using environmental DNA – a review of eDNA as a survey tool in ecology. J. Appl. Ecol. 51, 1450–1459 (2014).CAS 
    Article 

    Google Scholar 
    2.Palumbi, S. R. What can molecular genetics contribute to marine biogeography? An urchin’s tale. J. Exp. Mar. Biol. Ecol. 203, 75–92 (1996).CAS 
    Article 

    Google Scholar 
    3.Vucetich, J. A. & Waite, T. A. Spatial patterns of demography and genetic processes across the species’ range: null hypotheses for landscape conservation genetics. Conserv. Genet. 4(5), 639–645 (2003).Article 

    Google Scholar 
    4.Krishnamurthy, P. K. & Francis, R. A. A critical review on the utility of DNA barcoding in biodiversity conservation. Biodivers. Conserv. 21(8), 1901–1919 (2012).Article 

    Google Scholar 
    5.Metzker, M. L. Emerging technologies in DNA sequencing. Genome Res. 15(12), 1767–1776 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Gloor, G. B. et al. Microbiome Profiling by Illumina Sequencing of Combinatorial Sequence-Tagged PCR Products. PLoS ONE 5(10), e15406 (2010).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    7.Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. 108(1), 4516–4522 (2011).CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 
    8.Douglas, A. E. Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harb. Perspect. Biol. 6(2), a016113 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    9.Bolhuis, H. & Cretoiu, M. S. What is so special about marine microorganisms? Introduction to the marine microbiome—from diversity to biotechnological potential. In the Marine Microbiome (eds Stal, L. & Cretoiu, M.) (Springer, Cham, 2016).
    Google Scholar 
    10.Stal, L. & Cretoiu, M. S. (eds) The Marine Microbiome (Springer, 2016).
    Google Scholar 
    11.Huse, S. M. et al. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4(11), e1000255 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    12.Pedrós-Alió, C. The rare bacterial biosphere. Ann. Rev. Mar. Sci. 4, 449–466 (2012).PubMed 
    Article 

    Google Scholar 
    13.Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    14.Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71(2), 295–347 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Hentschel, U., Piel, J., Degnan, S. M. & Taylor, M. W. Genomic insights into the marine sponge microbiome. Nat. Rev. Microbiol. 10(9), 641–654 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Cleary, D. F. R. et al. The sponge microbiome within the greater coral reef microbial metacommunity. Nat. Commun. 10, 1644 (2019).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    17.León-Palmero, E. et al. Diversity and antimicrobial potential in sea anemone and holothurian microbiomes. PLoS One 13(5), e0196178 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Blasiak, L. C., Zinder, S. H., Buckley, D. H. & Russell, T. H. Bacterial diversity associated with the tunic of the model chordate Ciona intestinalis. ISME J. 8(2), 309–320 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Givens, C. E. et al. Comparison of the gut microbiome of 12 bony fish and 3 shark species. Mar. Ecol. Prog. Ser. 518, 209–223 (2015).Article 
    ADS 

    Google Scholar 
    20.Neu, A. T., Allen, E. E. & Roy, K. Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary. Environ. Microbiol. Rep. 11(3), 434–447 (2019).PubMed 
    Article 

    Google Scholar 
    21.Salazar, G. & Sunagawa, S. Marine microbial diversity. Curr. Biol. 27(11), 489–494 (2017).Article 
    CAS 

    Google Scholar 
    22.Dick, G. J. The microbiomes of deep-sea hydrothermal vents: distributed globally, shaped locally. Nat. Rev. Microbiol. 17(5), 271–283 (2019).CAS 
    PubMed 

    Google Scholar 
    23.Cavicchioli, R. Microbial ecology of Antarctic aquatic systems. Nat. Rev. Microbiol. 13, 691–706 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Zinger, L. et al. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6(9), e24570 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    25.Palumbi, S. & Hedgecock, D. The life of the sea: implications of marine population biology to conservation policy. In Marine conservation biology: the science of maintaining the sea’s biodiversity (eds Norse, E. A. & Crowder, L. B.) (Island Press, Washington, 2005).
    Google Scholar 
    26.Sousa, R., Delgado, J., González, J. A., Freitas, M. & Henriques, P. Marine snails of the genus Phorcus: Biology and ecology of sentinel species for human impacts on the rocky shores. In Biological Resources of Water (ed. Ray, S.) 141–167 (Croatia, IntechOpen., 2018).
    Google Scholar 
    27.Sousa, R. et al. Filling biological information gaps of the marine topshell Phorcus sauciatus (Gastropoda: Trochidae) to ensure its sustainable exploitation. J. Mar. Biol. Assoc. U.K. 99(4), 841–849 (2019).Article 

    Google Scholar 
    28.Sousa, R. et al. Disentangling exploitation of the intertidal grazer Phorcus sauciatus (Gastropoda: Trochidae) in an ocean archipelago: Implications for conservation. Mar. Ecol. 40(2), e12540 (2019).Article 
    ADS 

    Google Scholar 
    29.Donald, K. M. et al. Phylogenetic relationships elucidate colonization patterns in the intertidal grazers Osilinus Philippi, 1847 and Phorcus Risso, 1826 (Gastropoda: Trochidae) in the northeastern Atlantic Ocean and Mediterranean Sea. Mol. Phylogenet. Evol. 62(1), 35–45 (2012).PubMed 
    Article 

    Google Scholar 
    30.Takahashi, et al. Development of prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PLoS ONE 9(8), e105592 (2014).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    31.Herlemann, D. P. et al. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5(10), 1571–1579 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.QGIS Development Team. QGIS Geographic Information System (QGIS Association, 2020).33.Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Weiss, S. J. et al. Effects of library size variance, sparsity, and compositionality on the analysis of microbiome data. PeerJ PrePrints 3, e1157v1 (2015).
    Google Scholar 
    35.Staley, J. T. & Bauld, J. The genus Planctomyces. In The Prokaryotes (eds Starr, M. P. et al.) (Springer, Berlin, 1981).
    Google Scholar 
    36.Nelson, L. et al. Molecular analysis of gut microflora in captive-raised sea urchins (Lytechinus variegatus). J. World Aquaculture Soc. 41(5), 807–815 (2010).Article 

    Google Scholar 
    37.Hakim, J. A. et al. An abundance of Epsilonproteobacteria revealed in the gut microbiome of the laboratory cultured sea urchin, Lytechinus variegatus. Front. Microbiol. 6, 1047 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Moisander, P. H., Sexton, A. D. & Daley, M. C. Stable associations masked by temporal variability in the marine copepod microbiome. PLoS ONE 10(9), e0138967 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    39.Motarjemi, Y., Todd, E. & Moy, G. Encyclopedia of Food Safety (Elsevier, 2014).
    Google Scholar 
    40.Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32(5), 723–735 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Lokmer, A. & Wegner, K. M. Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. ISME J. 9(3), 670–682 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Lokmer, A. et al. Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales. Front. Microbiol. 7, 1367 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Kellogg, C. A., Goldsmith, D. B. & Gray, M. A. Biogeographic comparison of Lophelia-associated bacterial communities in the western Atlantic reveals conserved core microbiome. Front. Microbiol. 8, 796 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Burgsdorf, I. et al. Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Front. Microbiol. 5, 1–11 (2014).Article 

    Google Scholar 
    45.Kellogg, C. A. Microbiomes of stony and soft deep-sea corals share rare core bacteria. Microbiome 7, 90 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Hamdan, L. et al. Ocean currents shape the microbiome of Arctic marine sediments. ISME J. 7, 685–696 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Donaldson, G. P., Lee, S. M. & Mazmanian, S. K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14(1), 20–32 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Xiao, Y. et al. Comparative biogeography of the gut microbiome betweeen Jinhua and Landrace pigs. Sci. Rep. 8, 5985 (2018).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    49.Morelan, et al. Microbiome variation in an intertidal sea anemone across latitudes and symbiotic states. Front. Mar. Sci. 6, 7 (2019).Article 
    ADS 

    Google Scholar 
    50.Barton, E. D. Canary and Portugal currents. In Encyclopedia of Ocean Sciences (eds Steele, J. et al.) 380–389 (Academic Press, 2001).Chapter 

    Google Scholar 
    51.Spalding, M. D. et al. Marine ecoregions of the world: a bioregionalization of coast and shelf areas. BioScience 57, 573–583 (2007).Article 

    Google Scholar 
    52.Tuya, F. et al. Phytogeography of Lusitanian Macaronesia: biogeographic affinities in species richness and assemblage composition. Eur. J. Phycol. 44(3), 405–413 (2009).Article 

    Google Scholar 
    53.Freitas, R. et al. Restructuring of the “Macaronesia” biogeographic unit: A marine multi-taxon biogeographic approach. Sci. Rep. 9, 15792 (2019).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    54.Faria, J. et al. Disentangling the genetic and morphological structure of Patella candei complex in Macaronesia (NE Atlantic). Ecol. Evol. 7(16), 6125–6140 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Stramma, L. & Siedler, G. Seasonal changes in the North Atlantic subtropical gyre. J. Geophys. Res. Oceans 93(C7), 8111–8118 (1988).Article 
    ADS 

    Google Scholar 
    56.Mason, E. et al. Seasonal variability of the Canary current: a numerical study. J. Geophys. Res. 116(6), C06001 (2011).ADS 

    Google Scholar 
    57.Follows, M. J., Dutkiewicz, S., Grant, S. & Chisholm, S. W. Emergent biogeography of microbial communities in a model ocean. Science 315, 1843–1846 (2007).CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 
    58.Galand, P. E., Potvin, M., Casamayor, E. O. & Lovejoy, C. Hydrography shapes bacterial biogeography of the deep Arctic Ocean. ISME J. 4, 564–576 (2010).PubMed 
    Article 

    Google Scholar 
    59.Cicala, F., Cisterna-Céliz, J. A., Moore, J. D. & Rocha-Olivares, A. Structure, dynamics and predicted functional role of the gut microbiota of the blue (Haliotis fulgens) and yellow (H. corrugata) abalone from Baja California Sur. Mexico. PeerJ. 6, e5830 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    60.Gutiérrez-Díaz, I., Fernández-Navarro, T., Sánchez, B., Margolles, A. & González, S. Mediterranean diet and faecal microbiota: a transversal study. Food Funct. 7(5), 2347–2356 (2016).PubMed 
    Article 
    CAS 

    Google Scholar 
    61.Mueller, U. G. & Sachs, J. L. Engineering microbiomes to improve plant and animal health. Trends Microbiol. 23(10), 606–617 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Jost, L., Chao, A. & Chazdon, R. L. Compositional similarity and beta diversity. In Biological Diversity Frontiers in Measurement and Assessment (eds Magurran, A. E. & McGill, B. J.) (Oxford University Press, Oxford, 2011).
    Google Scholar  More

  • in

    Behavioral traits and territoriality in the symbiotic scaleworm Ophthalmonoe pettiboneae

    1.Baeza, J. A. & Thiel, M. Predicting territorial behavior in symbiotic crabs using host characteristics: A comparative study and proposal of a model. Mar. Biol. 142, 93–100. https://doi.org/10.1007/s00227-002-0927-1 (2003).Article 

    Google Scholar 
    2.Kamran, M. & Moore, P. A. Dominance and territory. In Encyclopedia of Evolutionary Psychological Science (eds Shackelford, T. K. & Weekes-Shackelford, V. A.) 1–4 (Springer, 2016).
    Google Scholar 
    3.Grant, J. W. A. Whether or not to defend? The influence of resource distribution. Mar. Behav. Physiol. 22, 137–153. https://doi.org/10.1080/10236249309378862 (1993).ADS 
    Article 

    Google Scholar 
    4.Duffy, J. E. The ecology and evolution of eusociality in sponge-dwelling shrimp. In Genes, Behaviors and Evolution of Social Insects (ed. Kikuchi, T.) 217–254 (Hokkaido University Press, 2002).
    Google Scholar 
    5.Baeza, J. A., Stotz, W. & Thiel, M. Agonistic behaviour and development of territoriality during ontogeny of the sea anemone dwelling crab Allopetrolisthes spinifrons (H. Milne Edwards, 1837)(Decapoda: Anomura: Porcellanidae). Mar. Freshw. Behav. Physiol. 35, 189–202. https://doi.org/10.1080/1023624021000003817 (2002).Article 

    Google Scholar 
    6.Castro, P. Symbiotic Brachyura. In Treatise on Zoology-Anatomy, Taxonomy, Biology. The Crustacea, Volume 9 Part C Vol. 2 (eds Castro, P. et al.) 543–581 (Brill, 2015).Chapter 

    Google Scholar 
    7.Wilson, E. O. Sociobiology: The New Synthesis (Harvard University, 1975).
    Google Scholar 
    8.Burt, W. H. Territoriality and home range concepts as applied to mammals. J. Mammal. 24, 346–352. https://doi.org/10.2307/1374834 (1943).Article 

    Google Scholar 
    9.Gerking, S. D. Feeding Ecology of Fish (Academic Press, 2014).
    Google Scholar 
    10.Barrows, E. M. Animal Behavior Desk Reference: A Dictionary of Animal Behavior, Ecology, and Evolution (CRC Press, 2000).Book 

    Google Scholar 
    11.Hardy, I. C. W. & Briffa, M. Animal Contests Vol. 357 (Cambridge University Press, 2013).Book 

    Google Scholar 
    12.Dimock, R. V. Jr. Intraspecific aggression and the distribution of a symbiotic polychaete on its host. In Symbiosis in the Sea (ed. Vernberg, W. B.) 29–44 (University of South Carolina Press, 1974).
    Google Scholar 
    13.Duffy, J. E., Morrison, C. L. & Macdonald, K. S. Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behav. Ecol. Sociobiol. 51, 488–495. https://doi.org/10.1007/s00265-002-0455-5 (2002).Article 

    Google Scholar 
    14.Huber, M. E. Aggressive behavior of Trapezia intermedia Miers and T. digitalis Latreille (Brachyura: Xanthidae). J. Crustacean Biol. 7, 238–248. https://doi.org/10.2307/1548604 (1987).Article 

    Google Scholar 
    15.Douglas, A. The Symbiotic Habit (Princeton University Press, 2010).
    Google Scholar 
    16.Williams, J. D. & McDermott, J. J. Hermit crab biocoenoses: A worldwide review of the diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 305, 1–128. https://doi.org/10.1016/j.jembe.2004.02.020 (2004).Article 

    Google Scholar 
    17.Fautin, D. G. The anemonefish symbiosis: What is known and what is not. Symbiosis 10, 23–46 (1991).
    Google Scholar 
    18.Martin, D. & Britayev, T. A. Symbiotic polychaetes: Review of known species. Oceanogr. Mar. Biol. Ann. Rev. 36, 217–340 (1998).
    Google Scholar 
    19.Fernández-Leborans, G. Epibiosis in Crustacea: An overview. Crustaceana 83, 549–640. https://doi.org/10.1163/001121610X532648 (2010).Article 

    Google Scholar 
    20.Stella, J. S., Pratchett, M. S., Hutchings, P. A. & Jones, G. P. Diversity, importance and vulnerability of coral-associated invertebrates. Oceanogr. Mar. Biol. Ann. Rev. 49, 43–116 (2011).
    Google Scholar 
    21.Thiel, M. & Baeza, J. A. Factors affecting the social behaviour of crustaceans living symbiotically with other marine invertebrates: a modelling approach. Symbiosis 30, 163–190 (2001).
    Google Scholar 
    22.Jones, K. M. M. The effect of territorial damselfish (family Pomacentridae) on the space use and behaviour of the coral reef fish Halichoeres bivittatus (Bloch, 1791) (family Labridae). J. Exp. Mar. Biol. Ecol. 324, 99–111. https://doi.org/10.1016/j.jembe.2005.04.009 (2005).Article 

    Google Scholar 
    23.Thiel, M., Zander, A. & Baeza, J. A. Movements of the symbiotic crab Liopetrolisthes mitra between its host sea urchin Tetrapygus niger. Bull. Mar. Sci. 72, 89–101 (2003).
    Google Scholar 
    24.Marin, I. & Britayev, T. A. Symbiotic Community Associated with Corals Galaxea Oken, 1815 (Euphillidae: Scleractinia) Vol. 148 (KMK Press, 2014).
    Google Scholar 
    25.Ross, R. M. Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Z. Tierpsychol. 46, 71–83. https://doi.org/10.1111/j.1439-0310.1978.tb01439.x (1978).Article 

    Google Scholar 
    26.Kobayashi, M. & Hattori, A. Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones. Ichthyol. Res. 53, 1–6. https://doi.org/10.1007/s10228-005-0305-3 (2006).Article 

    Google Scholar 
    27.Huebner, L. K., Dailey, B., Titus, B. M., Khalaf, M. & Chadwick, N. E. Host preference and habitat segregation among Red Sea anemonefish: Effects of sea anemone traits and fish life stages. Mar. Ecol. Progr. Ser. 464, 1–15. https://doi.org/10.3354/meps09964 (2012).ADS 
    Article 

    Google Scholar 
    28.Duffy, J. E. Eusociality in a coral-reef shrimp. Nature 381, 512–514. https://doi.org/10.1038/381512a0 (1996).ADS 
    CAS 
    Article 

    Google Scholar 
    29.Baeza, J. A. & Stotz, W. B. Host-use pattern and host-selection during ontogeny of the commensal crab Allopetrolisthes spinifrons (H. Milne Edwards, 1837) (Decapoda: Anomura: Porcellanidae). J. Nat. Hist. 35, 341–355. https://doi.org/10.1080/002229301300009586 (2001).Article 

    Google Scholar 
    30.Ambrosio, L. J. & Baeza, J. A. Territoriality and conflict avoidance explain asociality (solitariness) of the endosymbiotic pea crab Tunicotheres moseri. PLoS ONE 11, e0148285–e0148285. https://doi.org/10.1371/journal.pone.0148285 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Baeza, J. A. & Thiel, M. The mating system of symbiotic crustaceans: A conceptual model based on optimality and ecological constraints. In Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms (eds Duffy, J. E. & Thiel, M.) 250–267 (Oxford University Press, 2007).
    Google Scholar 
    32.Bell, J. L. Distribution and abundance of Dissodactylus mellitae Rathbun (Pinnotheridae) on Mellita quinquiesperforata (Leske)(Echinodermata). J. Exp. Mar. Biol. Ecol. 117, 93–114. https://doi.org/10.1016/0022-0981(88)90220-1 (1988).Article 

    Google Scholar 
    33.Castro, P. Movements between coral colonies in Trapezia ferruginea (Crustacea: Brachyura), an obligate symbiont of scleractinian corals. Mar. Biol. 46, 237–245. https://doi.org/10.1007/BF00390685 (1978).Article 

    Google Scholar 
    34.Baeza, J. A., Simpson, L., Ambrosio, L. J., Guéron, R. & Mora, N. Monogamy in a hyper-symbiotic shrimp. PLoS ONE 11, e0149797. https://doi.org/10.1371/journal.pone.0149797 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Diesel, R. Male-female association in the spider crab Inachus phalangium: The influence of female reproductive stage and size. J. Crustac. Biol. 8, 63–69. https://doi.org/10.1163/193724088X00080 (1988).Article 

    Google Scholar 
    36.Wells, H. W. & Wells, M. J. Observations on Pinnaxodes floridensis, a new species of pinnotherid crustacean commensal in holothurians. Bull. Mar. Sci. 11, 267–279 (1961).
    Google Scholar 
    37.Martin, D. & Britayev, T. A. Symbiotic polychaetes revisited: an update of the known species and relationships (1998–2017). Oceanogr. Mar. Biol. Ann. Rev. 56, 371–448. https://doi.org/10.1201/9780429454455-6 (2018).Article 

    Google Scholar 
    38.Perry, O., Sapir, Y., Perry, G., Ten Hove, H. & Fine, M. Substrate selection of Christmas tree worms (Spirobranchus spp.) in the Gulf of Eilat, Red Sea. J. Mar. Biol. Ass. UK 98, 791–799. https://doi.org/10.1017/S0025315416002022 (2018).Article 

    Google Scholar 
    39.Hunte, W., Colin, B. E. & Marsden, J. R. Habitat selection in the tropical polychaete Spirobranchus giganteus 1 Distribution on corals. Mar. Biol. 104, 87–92 (1990).Article 

    Google Scholar 
    40.Mackie, A. S. Y., Oliver, P. G. & Nygren, A. Antonbruunia sociabilis sp. nov (Annelida: Antonbruunidae) associated with the chemosynthetic deep-sea bivalve Thyasira scotiae Oliver & Drewery, 2014, and a re-examination of the systematic affinities of Antonbruunidae. Zootaxa 3995, 20–36 (2015).Article 

    Google Scholar 
    41.Ruff, R. E. A new species of Bathynoe (Polychaeta: Polynoidae) from the Northeast Pacific Ocean commensal with two species of deep-water asteroids. in: Systematics, Biology and Morphology of World Polychaeta. Proceedings of the Second International Polychaeta Conference. Ophelia Suppl. 5, 219–230 (1991).42.Miura, T. & Ohta, S. Two polychaete species from the deep-sea hydrothermal vent in the Middle Okinawa Trough. Zool. Sci. 8, 383–387 (1991).
    Google Scholar 
    43.Martin, D., Nygren, A., Hjelmstedt, P., Drake, P. & Gil, J. On the enigmatic symbiotic polychaete “Parasyllidea” humesi Pettibone, 1961 (Hesionidae): taxonomy, phylogeny and behaviour. Zool. J. Linn. Soc. 174, 429–446. https://doi.org/10.1111/zoj.12249 (2015).Article 

    Google Scholar 
    44.Chim, C. K., Ong, J. J. L. & Tan, K. S. An association between a hesionid polychaete and temnopleurid echinoids from Singapore. Cah. Biol. Mar. 54, 577–585. https://doi.org/10.21411/CBM.A.ED45E036 (2013).Article 

    Google Scholar 
    45.Goerke, H. Nereis fucata (Polychaeta, Nereidae) als kommensale von Eupagurus bernhardus (Crustacea, Decapoda) Entwicklung einer population und verhalten der art. Veröffentlichungen des Instituts für Meeresforschung in Bremerhaven 13, 79–81 (1971).
    Google Scholar 
    46.Britayev, T. A., Mekhova, E., Deart, Y. & Martin, D. Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae). PeerJ 5, e2930. https://doi.org/10.7717/peerj.2930 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Britayev, T. A., Martin, D., Krylova, E. M., von Cosel, R. & Aksiuk, E. S. Life-history traits of the symbiotic scale-worm Branchipolynoe seepensis and its relationships with host mussels of the genus Bathymodiolus from hydrothermal vents. Mar. Ecol. Evolut. Perspect. 28, 36–48. https://doi.org/10.1111/j.1439-0485.2007.00152.x (2007).Article 

    Google Scholar 
    48.Britayev, T. A. & Zamyshliak, E. A. Association of the commensal scaleworm Gastrolepidia clavigera (Polychaeta: Polynoidae) with holothurians near the coast of South Vietnam. Ophelia 45, 175–190 (1996).Article 

    Google Scholar 
    49.Britayev, T. A. Life cycle of the symbiotic scale-worm Arctonoe vittata (Polychaeta: Polynoidae). In: Systematics, Biology and Morphology of World Polychaeta. Proceedings of the Second International Polychaeta Conference. Ophelia Suppl. 5, 305–312 (1991).50.Devaney, D. M. An ectocommensal polynoid associated with Indo-pacific echinoderms, primarily ophiuroids. Occ. Pap. Bernice P. Bishop Mus. 23, 287–304 (1967).
    Google Scholar 
    51.Tokaji, H., Nakahara, K. & Goshima, S. Host switching improves survival rate of the symbiotic polychaete Arctonoe vittata. Plank. Bent. Res. 9, 189–196. https://doi.org/10.3800/pbr.9.189 (2014).Article 

    Google Scholar 
    52.Martin, D., Rosell, D. & Uriz, M. J. Harmothoe hyalonemae sp. nov. (Polychaeta, Polynoidae), an exclusive inhabitant of different Atlanto-Mediterranean species of Hyalonema (Porifera, Hexactinellida). Ophelia 35, 169–185 (1992).Article 

    Google Scholar 
    53.Reish, D. J. & Alosi, M. C. Aggressive behavior in the polychaetous annelid family Nereidae. Bull. South. Calif. Acad. Sci. 67, 21–28 (1968).
    Google Scholar 
    54.Evans, S. M. Behavior in polychaetes. Q. Rev. Biol. 46, 379–405 (1971).Article 

    Google Scholar 
    55.Scaps, P. Intraspecific agonistic behaviour in the polychaete Perinereis cultrifera (Grübe). Vie et Milieu 45, 123–128 (1995).
    Google Scholar 
    56.Johnson, H. P. A preliminary account of the marine annelids of the Pacific coast, with descriptions of new species. Proc. Calif. Acad. Sci. 1, 153–199 (1897).
    Google Scholar 
    57.Miers, E. J. Report on the Brachyura collected by HMS Challenger during the years 1873–1876. in: Report on the scientific results of the Voyage of HMS Challenger during the years 1873–76 under the command of Captain George S. Nares, R. N., F.R.S. and the late Captain Frank Tourle Thompson, R. N. Zoology 17, 1–363, pls. 361–329 (1886).58.Latreille, P. A. Trapezie. in Entomologie, ou histoire naturelle des crustaces, des arachnides et des insectes, Vol. 10 695–696 (Encyclopedie Methodique, Histoire Naturelle, 1828).59.Petersen, M. E. & Britayev, T. A. A new genus and species of polynoid scaleworm commensal with Chaetopterus appendiculatus Grube from the Banda Sea (Annelida: Polychaeta), with a review of commensals of Chaetopteridae. Bull. Mar. Sci. 60, 261–276 (1997).
    Google Scholar 
    60.Grube, A. E. Descriptiones Annulatorum novorum mare Ceylonicum habitantium ab honoratissimo Holdsworth collectorum. Proc. Zool. Soc. Lond. 41, 325–329. https://doi.org/10.1111/j.1096-3642.1874.tb02492.x (1874).Article 

    Google Scholar 
    61.Britayev, T. A. & Martin, D. Scale-worms (Polychaeta, Polynoidae) associated with chaetopterid worms (Polychaeta, Chaetopteridae), with description of a new genus and species. J. Nat. Hist. 39, 4081–4099. https://doi.org/10.1080/00222930600556229 (2005).Article 

    Google Scholar 
    62.Grant, J. W. A., Gaboury, C. L. & Levitt, H. L. Competitor-to-resource ratio, a general formulation of operational sex ratio, as a predictor of competitive aggression in Japanese medaka (Pisces: Oryziidae). Behav. Ecol. 11, 670–675. https://doi.org/10.1093/beheco/11.6.670 (2000).Article 

    Google Scholar 
    63.Britayev, T. A. & Smurov, A. V. Distribution and relocation of commensal crabs Pinnixa rathbhuni (Pinnotheridae) on their hosts. Dokl. Akad. Nauk SSSR 300, 1506–1509 (1988).
    Google Scholar 
    64.Walker, A. O. Notes on a collection of Crustacea from Singapore. J. Linn. Soc. Lond. Zool. 20, 107–117. https://doi.org/10.1111/j.1096-3642.1887.tb01440.x (1887).Article 

    Google Scholar 
    65.Kemp, D. J. Habitat selection and territoriality. In Insect behavior: from mechanisms to ecological and evolutionary consequences (eds Córdoba-Aguilar, A. et al.) 80–97 (Oxford University Press, 2018).
    Google Scholar 
    66.Jumars, P. A., Dorgan, K. M. & Lindsay, S. M. Diet of worms emended: An update of polychaete feeding guilds. Ann. Rev. Mar. Sci. 7, 497–520. https://doi.org/10.1146/annurev-marine-010814-020007 (2015).Article 
    PubMed 

    Google Scholar 
    67.Cotter, E., O’Riordan, R. M. & Myers, A. A. A histological study of reproduction in the serpulids Pomatoceros triqueter and Pomatoceros lamarckii (Annelida: Polychaeta). Mar. Biol. 142, 905–914 (2003).Article 

    Google Scholar 
    68.Prevedelli, D., Massamba N’Siala, G., Ansaloni, I. & Simonini, R. Life cycle of Marphysa sanguinea (Polychaeta: Eunicidae) in the Venice Lagoon (Italy). Mar. Ecol. 28, 384–393. https://doi.org/10.1111/j.1439-0485.2007.00160.x (2007).ADS 
    Article 

    Google Scholar 
    69.Bergman, D. A. & Moore, P. A. Prolonged exposure to social odours alters subsequent social interactions in crayfish (Orconectes rusticus). Anim. Behav. 70, 311–318. https://doi.org/10.1016/j.anbehav.2004.10.026 (2005).Article 

    Google Scholar 
    70.Arakaki, J. Y. et al. Battle of the borders: Is a range-extending fiddler crab affecting the spatial niche of a congener species?. J. Exp. Mar. Biol. Ecol. 532, 151445. https://doi.org/10.1016/j.jembe.2020.151445 (2020).Article 

    Google Scholar 
    71.Britayev, T. A. & Mekhova, E. S. Do symbiotic polychaetes migrate from host to host?. Mem. Mus. Victoria 71, 21–25 (2014).Article 

    Google Scholar 
    72.Livermore, J., Perreault, T. & Rivers, T. Luminescent defensive behaviors of polynoid polychaete worms to natural predators. Mar. Biol. 165, 149. https://doi.org/10.1007/s00227-018-3403-2 (2018).Article 

    Google Scholar 
    73.Daly, J. M. Segmentation, autotomy and regeneration of lost posterior segments in Harmothoe imbricata (L) (Polychaeta: Polynoidae). QH1.M454 1, 17–28 (1973).
    Google Scholar 
    74.Schiaparelli, S., Alvaro, M. C. & Barnich, R. Polynoid polychaetes living in the gut of irregular sea urchins: A first case of inquilinism in the Southern Ocean. Antarct. Sci. 23, 144–151. https://doi.org/10.1017/S0954102011000083 (2011).ADS 
    Article 

    Google Scholar 
    75.Sokal, R. R. & Rohlf, F. J. Biometry. The Principles and Practice of Statistics in Biological Research 3rd edn. (W.H. Freeman and Company, 1995).MATH 

    Google Scholar 
    76.Everitt, B. The Analysis of Contingency Tables 2nd edn. (Chapman & Hall, 1992).Book 

    Google Scholar  More

  • in

    Transcriptional response to prolonged perchlorate exposure in the methanogen Methanosarcina barkeri and implications for Martian habitability

    1.Krasnopolsky, V. A., Maillard, J. P. & Owen, T. C. Detection of methane in the martian atmosphere: evidence for life?. Icarus 172, 537–547 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    2.Formisano, V., Atreya, S., Encrenaz, T., Ignatiev, N. & Giuranna, M. Detection of methane in the atmosphere of mars. Science 306, 1758–1761 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Geminale, A., Formisano, V. & Giuranna, M. Methane in Martian atmosphere: average spatial, diurnal, and seasonal behaviour. Planet. Space Sci. 56, 1194–1203 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Mumma, M. J. et al. Strong release of methane on mars in northern summer 2003. Science 323, 1041–1045 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Webster, C. R. et al. Mars methane detection and variability at Gale crater. Science 347, 415–417 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Webster, C. R. et al. Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 360, 1093–1096 (2018).ADS 
    MathSciNet 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Korablev, O. et al. No detection of methane on Mars from early ExoMars Trace Gas Orbiter observations. Nature 568, 517–520 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Fries, M. et al. A cometary origin for martian atmospheric methane. Geochem. Perspect. Lett. 2, 10–23 (2016).Article 

    Google Scholar 
    9.Keppler, F. et al. Ultraviolet-radiation-induced methane emissions from meteorites and the Martian atmosphere. Nature 486, 93–96 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Moores, J. E. & Schuerger, A. C. UV degradation of accreted organics on Mars: IDP longevity, surface reservoir of organics, and relevance to the detection of methane in the atmosphere. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    11.Schuerger, A. C., Moores, J. E., Clausen, C. A., Barlow, N. G. & Britt, D. T. Methane from UV-irradiated carbonaceous chondrites under simulated Martian conditions. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    12.Etiope, G., Ehlmann, B. L. & Schoell, M. Low temperature production and exhalation of methane from serpentinized rocks on Earth: a potential analog for methane production on Mars. Icarus 224, 276–285 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    13.Oehler, D. Z. & Etiope, G. Methane seepage on mars: where to look and why. Astrobiology 17, 1233–1264 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Onstott, T. C. et al. Martian CH 4: sources, flux, and detection. Astrobiology 6, 377–395 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Elwood Madden, M. E., Ulrich, S. M., Onstott, T. C. & Phelps, T. J. Salinity-induced hydrate dissociation: A mechanism for recent CH4 release on Mars. Geophys. Res. Lett. https://doi.org/10.1029/2006GL029156 (2007).Article 

    Google Scholar 
    16.Conrad, R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ. Microbiol. Rep. 1, 285–292 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Kendrick, M. G. & Kral, T. A. Survival of methanogens during desiccation: implications for life on mars. Astrobiology 6, 546–551 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Anderson, K. L., Apolinario, E. E. & Sowers, K. R. Desiccation as a long-term survival mechanism for the archaeon Methanosarcina barkeri. Appl. Environ. Microbiol. 78, 1473–1479 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Kral, T. A. & Altheide, S. T. Methanogen survival following exposure to desiccation, low pressure and martian regolith analogs. Planet. Space Sci. 89, 167–171 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    20.Sowers, K. R. & Gunsalus, R. P. Adaptation for growth at various saline concentrations by the archaebacterium Methanosarcina thermophila. J. Bacteriol. 170, 998–1002 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Maestrojuan, G. M. et al. Taxonomy and halotolerance of mesophilic methanosarcina strains, assignment of strains to species, and synonymy of methanosarcina mazei and methanosarcina frisia. Int. J. Syst. Bacteriol. 42, 561–567 (1992).CAS 
    Article 

    Google Scholar 
    22.Sowers, K. R., Boone, J. E. & Gunsalus, R. P. Disaggregation of methanosarcina spp and growth as single cells at elevated osmolarity. Appl. Environ. Microbiol. 59, 3832–3839 (1993).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Sowers, K. R. & Gunsalus, R. P. Halotolerance in methanosarcina spp: Role of N(sup(epsilon))-Acetyl-(beta)-Lysine, (alpha)-Glutamate, Glycine Betaine, and K(sup+) as Compatible Solutes for Osmotic Adaptation. Appl. Environ. Microbiol. 61, 4382–4388 (1995).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Roessler, M. et al. Identification of a salt-induced primary transporter for glycine betaine in the methanogen methanosarcina mazei go1. Appl. Environ. Microbiol. 68, 2133–2139 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Shcherbakova, V., Oshurkova, V. & Yoshimura, Y. The effects of perchlorates on the permafrost methanogens: implication for autotrophic life on mars. Microorganisms 3, 518–534 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Kral, T. A. et al. Sensitivity and adaptability of methanogens to perchlorates: Implications for life on Mars. Planet. Space Sci. 120, 87–95 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Rivkina, E. M., Laurinavichus, K. S., Gilichinsky, D. A. & Shcherbakova, V. A. Methane generation in permafrost sediments. Dokl. Biol. Sci. https://doi.org/10.1023/A:1015366613580 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Rivkina, E. et al. Microbial life in permafrost. Adv. Sp. Res. 33, 1215–1221 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    29.Rivkina, E. et al. Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol. Ecol. 61, 1–15 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Takai, K. et al. Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. U. S. A. 105, 10949–10954 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Sinha, N., Nepal, S., Kral, T. & Kumar, P. Survivability and growth kinetics of methanogenic archaea at various pHs and pressures: implications for deep subsurface life on Mars. Planet. Space Sci. 136, 15–24 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    32.Chastain, B. K. & Kral, T. A. Approaching mars-like geochemical conditions in the laboratory: omission of artificial buffers and reductants in a study of biogenic methane production on a Smectite clay. Astrobiology 10, 889–897 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Kral, T. A., Altheide, T. S., Lueders, A. E. & Schuerger, A. C. Low pressure and desiccation effects on methanogens: Implications for life on Mars. Planet. Space Sci. 59, 264–270 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Mickol, R. L. & Kral, T. A. Low pressure tolerance by methanogens in an aqueous environment: implications for subsurface life on mars. Orig. Life Evol. Biosph. 47, 511–532 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nat. Rev. Microbiol. 2, 569–580 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Ericksen, G. E. The Chilean Nitrate Deposits: The origin of the Chilean nitrate deposits, which contain a unique group of saline minerals, has provoked lively discussion for more than 100 years. Am. Sci. 71, 366–374 (1983).ADS 

    Google Scholar 
    37.Kounaves, S. P. et al. Discovery of natural perchlorate in the antarctic dry valleys and its global implications. Environ. Sci. Technol. 44, 2360–2364 (2010).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Hecht, M. H. et al. Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science 325, 64–67 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Navarro-González, R., Vargas, E., de la Rosa, J., Raga, A. C. & McKay, C. P. Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars. J. Geophys. Res. 115, E12010 (2010).ADS 
    Article 

    Google Scholar 
    40.Glavin, D. P. et al. Evidence for perchlorates and the origin of chlorinated hydrocarbons detected by SAM at the Rocknest aeolian deposit in Gale Crater. J. Geophys. Res. Planets 118, 1955–1973 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Kounaves, S. P. et al. Identification of the perchlorate parent salts at the Phoenix Mars landing site and possible implications. Icarus 232, 226–231 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    42.Kounaves, S. P., Carrier, B. L., O’Neil, G. D., Stroble, S. T. & Claire, M. W. Evidence of martian perchlorate, chlorate, and nitrate in Mars meteorite EETA79001: Implications for oxidants and organics. Icarus 229, 206–213 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    43.Ojha, L. et al. Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat. Geosci. https://doi.org/10.1038/ngeo2546 (2015).Article 

    Google Scholar 
    44.Clark, B. C. & Kounaves, S. P. Evidence for the distribution of perchlorates on Mars. Int. J. Astrobiol. 15, 311–318 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Pestova, O. N., Myund, L. A., Khripun, M. K. & Prigaro, A. V. Polythermal study of the systems M(ClO4)2–H2O (M2+ = Mg2+, Ca2+, Sr2+, Ba2+). Russ. J. Appl. Chem. 78, 409–413 (2005).CAS 
    Article 

    Google Scholar 
    46.Chevrier, V. F., Hanley, J. & Altheide, T. S. Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site Mars. Geophys. Res. Lett. 36, L10202 (2009).ADS 
    Article 
    CAS 

    Google Scholar 
    47.Marion, G. M., Catling, D. C., Zahnle, K. J. & Claire, M. W. Modeling aqueous perchlorate chemistries with applications to Mars. Icarus 207, 675–685 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    48.Stillman, D. E. & Grimm, R. E. Dielectric signatures of adsorbed and salty liquid water at the Phoenix landing site Mars. J. Geophys. Res. 116, E09005 (2011).ADS 

    Google Scholar 
    49.Toner, J. D., Catling, D. C. & Light, B. The formation of supercooled brines, viscous liquids, and low-temperature perchlorate glasses in aqueous solutions relevant to Mars. Icarus 233, 36–47 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    50.Nikolakakos, G. & Whiteway, J. A. Laboratory investigation of perchlorate deliquescence at the surface of Mars with a Raman scattering lidar. Geophys. Res. Lett. 42, 7899–7906 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    51.Maeder, D. L. et al. The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes. J. Bacteriol. 188, 7922–7931 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Sorek, R. & Cossart, P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat. Rev. Genet. 11, 9–16 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Lobo, A. L. & Zinder, S. H. Diazotrophy and Nitrogenase Activity in the Archaebacterium Methanosarcina barkeri 227. Appl. Environ. Microbiol. 54, 1656–1661 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Lobo, A. L. & Zinder, S. H. Nitrogenase in the archaebacterium Methanosarcina barkeri 227. J. Bacteriol. 172, 6789–6796 (1990).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Kessler, P. S. & Leigh, J. A. Genetics of nitrogen regulation in Methanococcus maripaludis. Genetics 152, 1343–1351 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Kessler, P. S., Daniel, C. & Leigh, J. A. Ammonia Switch-Off of Nitrogen Fixation in the Methanogenic Archaeon Methanococcus maripaludis: Mechanistic Features and Requirement for the Novel GlnB Homologues, NifI1 and NifI2. J. Bacteriol. 183, 882–889 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Kempf, B. & Bremer, E. OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in bacillus subtilis. J. Biol. Chem. 270, 16701–16713 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Kempf, B. & Bremer, E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319–330 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Hoffmann, T. & Bremer, E. Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol. Chem. 398, 193–214 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Hippe, H., Caspari, D., Fiebig, K. & Gottschalk, G. Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Proc. Natl. Acad. Sci. 76, 494–498 (1979).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Kreisl, P. & Kandler, O. Chemical structure of the cell wall polymer of methanosarcina. Syst. Appl. Microbiol. 7, 293–299 (1986).CAS 
    Article 

    Google Scholar 
    62.Jarrell, K. F., Jones, G. M., Kandiba, L., Nair, D. B. & Eichler, J. S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications. Archaea 2010, 1–13 (2010).Article 
    CAS 

    Google Scholar 
    63.Srinivasan, G. Pyrrolysine encoded by UAG in archaea: charging of a UAG-decoding specialized tRNA. Science 296, 1459–1462 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Bin, P., Huang, R. & Zhou, X. Oxidation resistance of the sulfur amino acids: methionine and cysteine. Biomed Res. Int. 2017, 1–6 (2017).Article 
    CAS 

    Google Scholar 
    65.Armesto, X. L., Canle, L. M., Fernández, M. I., Garcı́a, M. V. & Santaballa, J. A. First steps in the oxidation of sulfur-containing amino acids by hypohalogenation: very fast generation of intermediate sulfenyl halides and halosulfonium cations. Tetrahedron 56, 1103–1109 (2000).CAS 
    Article 

    Google Scholar 
    66.Casanueva, A., Tuffin, M., Cary, C. & Cowan, D. A. Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol. 18, 374–381 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Oren, A. Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie Van Leeuwenhoek 58, 291–298 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Seibel, B. A. & Walsh, P. J. Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol. 205, 297–306 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Lobo, A. L. & Zinder, S. H. Nitrogen fixation by methanogenic bacteria. in Biological Nitrogen Fixation (eds. Stacey, G., Burris, R. H. & Evans, H. J.) 191–211 (Chapman and Hall, 1992).70.Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9, 499–508 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Bardiya, N. & Bae, J.-H. Dissimilatory perchlorate reduction: A review. Microbiol. Res. 166, 237–254 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Barnum, T. P. et al. Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities. ISME J. 12, 1568–1581 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Oren, A., Elevi, B. R. & Mana, L. Perchlorate and halophilic prokaryotes: implications for possible halophilic life on Mars. Extremophiles 18, 75–80 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Liebensteiner, M. G., Pinkse, M. W. H., Schaap, P. J., Stams, A. J. M. & Lomans, B. P. Archaeal (Per)Chlorate reduction at high temperature: an interplay of biotic and abiotic reactions. Science 340, 85–87 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    75.Bender, K. S. et al. Identification, characterization, and classification of genes encoding perchlorate reductase. J. Bacteriol. 187, 5090–5096 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Youngblut, M. D. et al. Perchlorate reductase is distinguished by active site aromatic gate residues. J. Biol. Chem. 291, 9190–9202 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Okeke, B. C., Giblin, T. & Frankenberger, W. T. Reduction of perchlorate and nitrate by salt tolerant bacteria. Environ. Pollut. https://doi.org/10.1016/S0269-7491(01)00288-3 (2002).Article 
    PubMed 

    Google Scholar 
    78.He, L. et al. Biological perchlorate reduction: which electron donor we can choose?. Environ. Sci. Pollut. Res. 26, 16906–16922 (2019).CAS 
    Article 

    Google Scholar 
    79.Xie, T. et al. Perchlorate bioreduction linked to methane oxidation in a membrane biofilm reactor: performance and microbial community structure. J. Hazard. Mater. https://doi.org/10.1016/j.jhazmat.2018.06.011 (2018).Article 
    PubMed 

    Google Scholar 
    80.Chaudhuri, S. K., O’Connor, S. M., Gustavson, R. L., Achenbach, L. A. & Coates, J. D. Environmental factors that control microbial perchlorate reduction. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.68.9.4425-4430.2002 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Abu-Omar, M. M. Effective and catalytic reduction of perchlorate by atom transfer-reaction kinetics and mechanisms. Comments Inorg. Chem. 24, 15–37 (2003).CAS 
    Article 

    Google Scholar 
    82.Adkins, H. & Cramer, H. I. The use of nickel as a catalyst for hydrogenation. J. Am. Chem. Soc. 52, 4349–4358 (1930).CAS 
    Article 

    Google Scholar 
    83.Thauer, R. K. et al. Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu. Rev. Biochem. 79, 507–536 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Zhang, H., Bruns, M. A. & Logan, B. E. Perchlorate reduction by a novel chemolithoautotrophic, hydrogen-oxidizing bacterium. Environ. Microbiol. https://doi.org/10.1046/j.1462-2920.2002.00338.x (2002).Article 
    PubMed 

    Google Scholar 
    85.Ide, T., Bäumer, S. & Deppenmeier, U. Energy conservation by the H2: heterodisulfide oxidoreductase from methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol. 181, 4076–4080 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Deppenmeier, U. The membrane-bound electron transport system of methanosarcina species. J. Bioenerg. Biomembr. 36, 55–64 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R. & Metcalf, W. W. Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc. Natl. Acad. Sci. 99, 5632–5637 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Kulkarni, G., Mand, T. D. & Metcalf, W. W. Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri. MBio 9, (2018).89.Bobik, T. Formyl-methanofuran synthesis in Methanobacterium thermoautotrophicum. FEMS Microbiol. Lett. 87, 323–326 (1990).CAS 
    Article 

    Google Scholar 
    90.Wang, D. M., Shah, S. I., Chen, J. G. & Huang, C. P. Catalytic reduction of perchlorate by H2 gas in dilute aqueous solutions. Sep. Purif. Technol. 60, 14–21 (2008).CAS 
    Article 

    Google Scholar 
    91.Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579–591 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    92.Mand, T. D. & Metcalf, W. W. Energy Conservation and Hydrogenase Function in Methanogenic Archaea, in Particular the Genus Methanosarcina. Microbiol. Mol. Biol. Rev. 83, (2019).93.Rummel, J. D. et al. A new analysis of mars “special regions”: findings of the second MEPAG special regions science analysis group (SR-SAG2). Astrobiology 14, 887–968 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    94.Bryant, M. P. & Boone, D. R. Emended description of strain MST(DSM 800T), the type strain of methanosarcina barkeri. Int. J. Syst. Bacteriol. 37, 169–170 (1987).Article 

    Google Scholar 
    95.Widdel, F., Kohring, G.-W. & Mayer, F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Arch. Microbiol. 134, 286–294 (1983).CAS 
    Article 

    Google Scholar 
    96.Francisco, D. E., Mah, R. A. & Rabin, A. C. Acridine orange-epifluorescence technique for counting bacteria in natural waters. Trans. Am. Microsc. Soc. 92, 416 (1973).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.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 
    98.Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    99.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    100.Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    101.Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    102.Love, M., Anders, S. & Huber, W. Differential analysis of count data–the DESeq2 package. Genome Biol. 15, 10–1186 (2014).Article 
    CAS 

    Google Scholar 
    103.Ogata, H. et al. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27, 29–34 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish

    1.Clobert, J., Baguette, M., Benton, T. G. & Bullock, J. M. Dispersal Ecology and Evolution (Oxford University Press, 2012).Book 

    Google Scholar 
    2.Paris, C. B. & Cowen, R. K. Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol. Oceanogr. 49, 1964–1979 (2004).ADS 
    Article 

    Google Scholar 
    3.Roberts, C. M. Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457 (1997).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Fisher, R. & Wilson, S. K. Maximum sustainable swimming speeds of late-stage larvae of nine species of reef fishes. J. Exp. Mar. Biol. Ecol. 312, 171–186 (2004).Article 

    Google Scholar 
    5.Fisher, R., Leis, J. M., Clark, D. L. & Wilson, S. K. Critical swimming speeds of late-stage coral reef fish larvae: variation within species, among species and between locations. Mar. Biol. 147, 1201–1212 (2005).Article 

    Google Scholar 
    6.Leis, J. M. Ontogeny of behaviour in larvae of marine demersal fishes. Ichthyol. Res. 57, 325–342 (2010).Article 

    Google Scholar 
    7.Faillettaz, R., Durand, E., Paris, C. B., Koubbi, P. & Irisson, J.-O. Swimming speeds of Mediterranean settlement-stage fish larvae nuance Hjort’s aberrant drift hypothesis. Limnol. Oceanogr. 63, 509–523 (2018).ADS 
    Article 

    Google Scholar 
    8.Majoris, J. E., Catalano, K. A., Scolaro, D., Atema, J. & Buston, P. M. Ontogeny of larval swimming abilities in three species of coral reef fishes and a hypothesis for their impact on the spatial scale of dispersal. Mar. Biol. 166, 159 (2019).Article 

    Google Scholar 
    9.Leis, J. M., Sweatman, H. P. & Reader, S. E. What the pelagic stages of coral reef fishes are doing out in blue water: daytime field observations of larval behavioural capabilities. Mar. Freshw. Res. 47, 401–411 (1996).Article 

    Google Scholar 
    10.Leis, J., Paris, C., Irisson, J., Yerman, M. & Siebeck, U. Orientation of fish larvae in situ is consistent among locations, years and methods, but varies with time of day. Mar. Ecol. Prog. Ser. 505, 193–208 (2014).ADS 
    Article 

    Google Scholar 
    11.Leis, J. M. & Carson-Ewart, B. M. Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar. Ecol. Prog. Ser. 252, 239–253 (2003).ADS 
    Article 

    Google Scholar 
    12.Paris, C. B., Guigand, C. M., Irisson, J.-O., Fisher, R. & D’Alessandro, E. Orientation with no frame of reference (OWNFOR): a novel system to observe and quantify orientation in reef fish larvae. In Caribbean Connectivity: Implications for Marine Protected Area Management 52–62 (2008).13.Rossi, A., Irisson, J.-O., Levaray, M., Pasqualini, V. & Agostini, S. Orientation of Mediterranean fish larvae varies with location. Mar. Biol. 166, 100 (2019).Article 

    Google Scholar 
    14.Simpson, S. D., Meekan, M., Montgomery, J., McCauley, R. & Jeffs, A. Homeward sound. Science 308, 221–221 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Leis, J. M., Siebeck, U. & Dixson, D. L. How nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integr. Comp. Biol. 51, 826–843 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Paris, C. B. et al. Reef odor: a wake up call for navigation in reef fish larvae. PLoS ONE 8, e72808 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Mouritsen, H., Atema, J., Kingsford, M. J. & Gerlach, G. Sun compass orientation helps coral reef fish larvae return to their natal reef. PLoS ONE 8, e66039 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Berenshtein, I. et al. Polarized light sensitivity and orientation in coral reef fish post-larvae. PLoS ONE 9, e88468 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    19.Bottesch, M. et al. A magnetic compass that might help coral reef fish larvae return to their natal reef. Curr. Biol. 26, R1266–R1267 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Cresci, A., Allan, B. J. M., Shema, S. D., Skiftesvik, A. B. & Browman, H. I. Orientation behavior and swimming speed of Atlantic herring larvae (Clupea harengus) in situ and in laboratory exposures to rotated artificial magnetic fields. J. Exp. Mar. Biol. Ecol. 526, 151358 (2020).Article 

    Google Scholar 
    21.Faillettaz, R., Paris, C. B. & Irisson, J.-O. Larval fish swimming behavior alters dispersal patterns from marine protected areas in the North-Western Mediterranean Sea. Front. Mar. Sci. 5, 97 (2018).Article 

    Google Scholar 
    22.Staaterman, E., Paris, C. B. & Helgers, J. Orientation behavior in fish larvae: a missing piece to Hjort’s critical period hypothesis. J. Theor. Biol. 304, 188–196 (2012).PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 
    23.Lara, M. R. Development of the nasal olfactory organs in the larvae, settlement-stages and some adults of 14 species of Caribbean reef fishes (Labridae, Scaridae, Pomacentridae). Mar. Biol. 154, 51–64 (2008).Article 

    Google Scholar 
    24.Arvedlund, M. & Kavanagh, K. The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems. In Ecological Connectivity among Tropical Coastal Ecosystems (ed. Nagelkerken, I.) 135–184 (Springer, 2009).Chapter 

    Google Scholar 
    25.Teodósio, M. A., Paris, C. B., Wolanski, E. & Morais, P. Biophysical processes leading to the ingress of temperate fish larvae into estuarine nursery areas: a review. Estuar. Coast. Shelf Sci. 183, 187–202 (2016).ADS 
    Article 

    Google Scholar 
    26.Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology. J. Fish Biol. 95, 311–323 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Nickles, K. R., Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Organization and ontogeny of a complex lateral line system in a Goby (Elacatinus lori), with a consideration of function and ecology. Copeia 108, 863–885 (2020).Article 

    Google Scholar 
    28.Fuiman, L., Higgs, D. & Poling, K. Changing structure and function of the ear and lateral line system of fishes during development. Am. Fish. Soc. Symp. 2004, 117–144 (2004).
    Google Scholar 
    29.Blaxter, J. H. S. Light intensity, vision, and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293–307 (1968).Article 

    Google Scholar 
    30.Blaxter, J. H. S. & Hoss, D. E. The effect of rapid changes of hydrostatic pressure on the Atlantic herring Clupea harengus L. II. The response of the auditory bulla system in larvae and juveniles. J. Exp. Mar. Biol. Ecol. 41, 87–100 (1979).Article 

    Google Scholar 
    31.Colin, P. L. A new species of sponge-dwelling Elacatinus (Pisces: Gobiidae) from the western Caribbean. Zootaxa 106, 1–7 (2002).Article 

    Google Scholar 
    32.Colin, P. L. Fishes as living tracers of connectivity in the tropical western North Atlantic: I. Distribution of the neon gobies, genus Elacatinus (Pisces: Gobiidae). Zootaxa 2370, 36–52 (2010).Article 

    Google Scholar 
    33.Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.D’Aloia, C. C., Majoris, J. E. & Buston, P. M. Predictors of the distribution and abundance of a tube sponge and its resident goby. Coral Reefs 30, 777 (2011).ADS 
    Article 

    Google Scholar 
    35.Majoris, J. E., Francisco, F. A., Atema, J. & Buston, P. M. Reproduction, early development, and larval rearing strategies for two sponge-dwelling neon gobies, Elacatinus lori and E. colini. Aquaculture 483, 286–295 (2018).Article 

    Google Scholar 
    36.D’Aloia, C. C. et al. Patterns, causes, and consequences of marine larval dispersal. Proc. Natl. Acad. Sci. 112, 13940–13945 (2015).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    37.Majoris, J. E., D’Aloia, C. C., Francis, R. K. & Buston, P. M. Differential persistence favors habitat preferences that determine the distribution of a reef fish. Behav. Ecol. 29, 429–439 (2018).Article 

    Google Scholar 
    38.Chaput, R., Majoris, J. E., Guigand, C. M., Huse, M. & D’Alessandro, E. K. Environmental conditions and paternal care determine hatching synchronicity of coral reef fish larvae. Mar. Biol. 166, 118 (2019).Article 
    CAS 

    Google Scholar 
    39.D’Aloia, C., Xuereb, A., Fortin, M., Bogdanowicz, S. & Buston, P. Limited dispersal explains the spatial distribution of siblings in a reef fish population. Mar. Ecol. Prog. Ser. 607, 143–154 (2018).ADS 
    Article 

    Google Scholar 
    40.Williamson, D. H. et al. Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park. Mol. Ecol. 25, 6039–6054 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Almany, G. R. et al. Larval fish dispersal in a coral-reef seascape. Nat. Ecol. Evol. 1, 0148 (2017).Article 

    Google Scholar 
    42.Bode, M. et al. Successful validation of a larval dispersal model using genetic parentage data. PLOS Biol. 17, e3000380 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Nakae, M., Asaoka, R., Wada, H. & Sasaki, K. Fluorescent dye staining of neuromasts in live fishes: an aid to systematic studies. Ichthyol. Res. 59, 286–290 (2012).Article 

    Google Scholar 
    44.Webb, J. F. & Shirey, J. E. Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish. Dev. Dyn. 228, 370–385 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Becker, E. A., Bird, N. C. & Webb, J. F. Post-embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes. J. Morphol. 277, 1273–1291 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Webb, J. F. Morphological diversity, development, and evolution of the mechanosensory lateral line system. In The Lateral Line System (eds Coombs, S. et al.) 17–72 (Springer, 2014). https://doi.org/10.1007/2506_2013_12.Chapter 

    Google Scholar 
    47.Asaoka, R., Nakae, M. & Sasaki, K. The innervation and adaptive significance of extensively distributed neuromasts in Glossogobius olivaceus (Perciformes: Gobiidae). Ichthyol. Res. 59, 143–150 (2011).Article 

    Google Scholar 
    48.Asaoka, R., Nakae, M. & Sasaki, K. Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobioids (Perciformes: Rhyacichthyidae). Ichthyol. Res. 61, 49–58 (2014).Article 

    Google Scholar 
    49.Nickles, K. Ontogeny of the lateral line and visual systems of a Caribbean Reef Goby, Elacatinus lori (University of Rhode Island, 2019).50.Shand, J., Døving, K. B. & Collin, S. P. Optics of the developing fish eye: comparisons of Matthiessen’s ratio and the focal length of the lens in the black bream Acanthopagrus butcheri (Sparidae, Teleostei). Vis. Res. 39, 1071–1078 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Webb, J. F. et al. Development of the ear, hearing capabilities and laterophysic connection in the spotfin butterflyfish (Chaetodon ocellatus). Environ. Biol. Fishes 95, 275–290 (2012).Article 

    Google Scholar 
    52.Popper, A. N. & Hoxter, B. Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hear. Res. 15, 133–142 (1984).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Bever, M. M. & Fekete, D. M. Atlas of the developing inner ear in zebrafish. Dev. Dyn. 223, 536–543 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Haddon, C. & Lewis, J. Early ear development in the embryo of the Zebrafish, Danio rerio. J. Comp. Neurol. 365, 113–128 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Kawamura, G. et al. Morphogenesis of sense organs in the bluefin tuna Thunnus orientalis. in The Big Fish Bang Proceedings of the 26th Annual Larval Fish Conference (eds Browman, H. & Skiftesvik, A. B.) 123–135 (2003).
    Google Scholar 
    56.Pankhurst, P. M. & Butler, P. Development of the sensory organs in the greenback flounder, Rhombosolea tapirina. Mar. Freshw. Behav. Physiol. 28, 55–73 (1996).Article 

    Google Scholar 
    57.Lara, M. R. Morphology of the eye and visual acuities in the settlement-intervals of some Coral Reef Fishes (Labridae, Scaridae). Environ. Biol. Fishes 62, 365–378 (2001).Article 

    Google Scholar 
    58.Lara, M. R. Sensory Development in Settlement-Stage Larvae of Caribbean Labrids and Scarids: A Comparative Study with Implications for Ecomorphology and Life History Strategies (College of William and Mary, 1999).
    Google Scholar 
    59.Lecchini, D., Planes, S. & Galzin, R. Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav. Ecol. Sociobiol. 58, 18–26 (2005).Article 

    Google Scholar 
    60.Dixson, D. L. et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish. Oecologia 174, 99–107 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Irisson, J.-O., Guigand, C. & Paris, C. B. Detection and quantification of marine larvae orientation in the pelagic environment. Limnol. Oceanogr. Methods 7, 664–672 (2009).Article 

    Google Scholar 
    62.Irisson, J.-O., Paris, C. B., Leis, J. M. & Yerman, M. N. With a little help from my friends: group orientation by larvae of a coral reef fish. PLoS ONE 10, e0144060 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    63.Faillettaz, R., Blandin, A., Paris, C. B., Koubbi, P. & Irisson, J.-O. Sun-compass orientation in Mediterranean fish larvae. PLoS ONE 10, e0135213 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Lindo-Atichati, D., Curcic, M., Paris, C. B. & Buston, P. M. Description of surface transport in the region of the Belizean Barrier Reef based on observations and alternative high-resolution models. Ocean Model 106, 74–89 (2016).ADS 
    Article 

    Google Scholar 
    65.Agostinelli, C. & Lund, U. R package ‘circular’: Circular Statistics (version 0.4-93). https://r-forge.r-project.org/projects/circular/ (2017).66.R Core Team. R: A language and environment for statistical computing (R Found Stat Comput, 2013).
    Google Scholar 
    67.Leis, J., Hay, A. & Howarth, G. Ontogeny of in situ behaviours relevant to dispersal and population connectivity in larvae of coral-reef fishes. Mar. Ecol. Prog. Ser. 379, 163–179 (2009).ADS 
    Article 

    Google Scholar 
    68.Leis, J. M. & Carson-Ewart, B. M. (eds) The larvae of Indo-Pacific coastal fishes: an identification guide to marine fish larvae, 2nd edn. (Brill, 2004).
    Google Scholar 
    69.Kingsford, M. J. et al. Sensory environments, larval abilities and local self-recruitment. Bull. Mar. Sci. 70, 309–340 (2002).
    Google Scholar 
    70.Cresci, A. et al. Atlantic haddock (Melanogrammus aeglefinus) larvae have a magnetic compass that guides their orientation. iScience 19, 1173–1178 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl. Acad. Sci. 104, 858–863 (2007).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Dixson, D. L. et al. Coral reef fish smell leaves to find island homes. Proc. R. Soc. B Biol. Sci. 275, 2831–2839 (2008).Article 

    Google Scholar 
    73.Berenshtein, I. et al. Auto-correlated directional swimming can enhance settlement success and connectivity in fish larvae. J. Theor. Biol. 439, 76–85 (2018).MathSciNet 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Shaw, A. K., D’Aloia, C. C. & Buston, P. M. The evolution of marine larval dispersal kernels in spatially structured habitats: analytical models, individual-based simulations, and comparisons with empirical estimates. Am. Nat. 193, 424–435 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Ronce, O. & Clobert, J. Dispersal syndromes. In Dispersal Ecology and Evolution Vol. 55 (eds Clobert, J. et al.) 119–138 (Oxford University Press, Oxford, 2012).Chapter 

    Google Scholar 
    77.Huebert, K. & Sponaugle, S. Observed and simulated swimming trajectories of late-stage coral reef fish larvae off the Florida Keys. Aquat. Biol. 7, 207–216 (2009).Article 

    Google Scholar 
    78.Hamilton, W. D. & May, R. M. Dispersal in stable habitats. Nature 269, 578–581 (1977).ADS 
    Article 

    Google Scholar 
    79.Leis, J. et al. In situ orientation of fish larvae can vary among regions. Mar. Ecol. Prog. Ser. 537, 191–203 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    80.Botsford, L. W. et al. Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28, 327–337 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.White, J. W., Botsford, L. W., Hastings, A. & Largier, J. L. Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal. Mar. Ecol. Prog. Ser. 398, 49–67 (2010).ADS 
    Article 

    Google Scholar 
    82.Green, A. L. et al. Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design: connectivity and marine reserves. Biol. Rev. https://doi.org/10.1111/brv.12155 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    83.Munguia-Vega, A. et al. Ecological guidelines for designing networks of marine reserves in the unique biophysical environment of the Gulf of California. Rev. Fish Biol. Fish. 28, 749–776 (2018).Article 

    Google Scholar 
    84.Cowen, R. K., Paris, C. B. & Srinivasan, A. Scaling of connectivity in marine populations. Science 311, 522–527 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    85.Paris, C. B., Chérubin, L. M. & Cowen, R. K. Surfing, spinning, or diving from reef to reef: effects on population connectivity. Mar. Ecol. Prog. Ser. 347, 285–300 (2007).ADS 
    Article 

    Google Scholar 
    86.Mann, D. A., Casper, B. M., Boyle, K. S. & Tricas, T. C. On the attraction of larval fishes to reef sounds. Mar. Ecol. Prog. Ser. 338, 307–310 (2007).ADS 
    Article 

    Google Scholar 
    87.Esri. World Imagery [basemap]. 500m. Imagery, basemaps, and land cover. May 14, 2020. https://www.arcgis.com/home/webmap/viewer.html. (2020). More

  • in

    Short term fluctuating temperature alleviates Daphnia stoichiometric constraints

    1.Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article 

    Google Scholar 
    2.Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706. https://doi.org/10.1038/nature09407 (2010).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Elser, J. J. et al. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3, 540–550 (2000).Article 

    Google Scholar 
    4.Elser, J., Obrien, W., Dobberfuhl, D. & Dowling, T. The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J. Evol. Biol. 13, 845–853 (2000).Article 

    Google Scholar 
    5.Hessen, D. O., Elser, J. J., Sterner, R. W. & Urabe, J. Ecological stoichiometry: An elementary approach using basic principles. Limnol. Oceanogr. 58, 2219–2236 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    6.Hessen, D. O., Faerovig, P. J. & Andersen, T. Light, nutrients, and P : C ratios in algae: Grazer performance related to food quality and quantity. Ecology 83, 1886–1898 (2002).Article 

    Google Scholar 
    7.Moody, E. K., Rugenski, A. T., Sabo, J. L., Turner, B. L. & Elser, J. J. Does the growth rate hypothesis apply across temperatures? Variation in the growth rate and body phosphorus of neotropical benthic grazers. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2017.00014 (2017).Article 

    Google Scholar 
    8.Prater, C., Wagner, N. D. & Frost, P. C. Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations. Limnol. Oceanogr. 63, 1727–1740. https://doi.org/10.1002/lno.10803 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Boersma, M. et al. Temperature driven changes in the diet preference of omnivorous copepods: No more meat when it’s hot?. Ecol. Lett. 19, 45–53. https://doi.org/10.1111/ele.12541 (2016).Article 
    PubMed 

    Google Scholar 
    10.Wojewodzic, M. W., Kyle, M., Elser, J. J., Hessen, D. O. & Andersen, T. Joint effect of phosphorus limitation and temperature on alkaline phosphatase activity and somatic growth in Daphnia magna. Oecologia 165, 837–846. https://doi.org/10.1007/s00442-010-1863-2 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    11.Starke, C. W. E., Jones, C. L. C., Burr, W. S. & Frost, P. C. Interactive effects of water temperature and stoichiometric food quality on Daphnia pulicaria. Freshwat. Biol. 66, 256–265. https://doi.org/10.1111/fwb.13633 (2020).CAS 
    Article 

    Google Scholar 
    12.Ruiz, T. et al. U-shaped response Unifies views on temperature dependency of stoichiometric requirements. Ecol. Lett. 23, 860–869. https://doi.org/10.1111/ele.13493 (2020).Article 
    PubMed 

    Google Scholar 
    13.Persson, J., Wojewodzic, M. W., Hessen, D. O. & Andersen, T. Increased risk of phosphorus limitation at higher temperatures for Daphnia magna. Oecologia 165, 123–129. https://doi.org/10.1007/s00442-010-1756-4 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    14.Malzahn, A. M., Doerfler, D. & Boersma, M. Junk food gets healthier when it’s warm. Limnol. Oceanogr. 61, 1677–1685. https://doi.org/10.1002/lno.10330 (2016).ADS 
    Article 

    Google Scholar 
    15.Cross, W. F., Hood, J. M., Benstead, J. P., Huryn, A. D. & Nelson, D. Interactions between temperature and nutrients across levels of ecological organization. Glob. Change Biol. 21, 1025–1040. https://doi.org/10.1111/gcb.12809 (2015).ADS 
    Article 

    Google Scholar 
    16.Woods, H. A. et al. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17, 237–245. https://doi.org/10.1046/j.1365-2435.2003.00724.x (2003).Article 

    Google Scholar 
    17.Cotner, J. B., Makino, W. & Biddanda, B. A. Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26–33. https://doi.org/10.1007/s00248-006-9040-1 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Hessen, D. O. et al. Changes in stoichiometry, cellular RNA, and alkaline phosphatase activity of Chlamydomonas in response to temperature and nutrients. Front. Microbiol. 8, 18. https://doi.org/10.3389/fmicb.2017.00018 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Van Geest, G. J., Sachse, R., Brehm, M., van Donk, E. & Hessen, D. Maximizing growth rate at low temperatures: RNA:DNA allocation strategies and life history traits of Arctic and temperate Daphnia. Polar Biol. 33, 1255–1262 (2010).Article 

    Google Scholar 
    20.Prater, C., Wagner, N. D. & Frost, P. C. Interactive effects of genotype and food quality on consumer growth rate and elemental content. Ecology 98, 1399–1408. https://doi.org/10.1002/ecy.1795 (2017).Article 
    PubMed 

    Google Scholar 
    21.Lampert, W. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3, 21–27 (1989).Article 

    Google Scholar 
    22.Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P. & Breckenridge, J. K. Towards a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnol. Oceanogr. 56, 1603–1623 (2011).ADS 
    Article 

    Google Scholar 
    23.Dawidowicz, P. & Loose, C. J. Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol. Oceanogr. 37, 1589–1595 (1992).ADS 
    Article 

    Google Scholar 
    24.Mikulski, A., Grzesiuk, M., Rakowska, A., Bernatowicz, P. & Pijanowska, J. Thermal shock in Daphnia: cost of diel vertical migrations or inhabiting thermally-unstable waterbodies?. Fund. Appl. Limnol. 190, 213–220. https://doi.org/10.1127/fal/2017/0989 (2017).Article 

    Google Scholar 
    25.Reichwaldt, E. S., Wolf, I. D. & Stibor, H. Effects of a fluctuating temperature regime experienced by Daphnia during diel vertical migration on Daphnia life history parameters. Hydrobiologia 543, 199–205. https://doi.org/10.1007/s10750-004-7451-x (2005).Article 

    Google Scholar 
    26.Orcutt, J. D. & Porter, K. G. Diel vertical migration in zooplankton. Constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol. Oceanogr. 28, 720–730 (1983).ADS 
    Article 

    Google Scholar 
    27.Stich, H. B. & Lampert, W. Growth and reproduction of migrating and non-migrating Daphnia species under simulated food and temperature conditions of diurnal vertical migration. Oecologia 61, 192–196. https://doi.org/10.1007/BF00396759 (1984).ADS 
    Article 
    PubMed 

    Google Scholar 
    28.Fischer, J. M. et al. Diel vertical migration of copepods in mountain lakes: The changing role of ultraviolet radiation across a transparency gradient. Limnol. Oceanogr. 60, 252–262. https://doi.org/10.1002/lno.10019 (2015).ADS 
    Article 

    Google Scholar 
    29.Kessler, K., Lockwood, R. S., Williamson, C. E. & Saros, J. E. Vertical distribution of zooplankton in subalpine and alpine lakes: Ultraviolet radiation, fish predation, and the transparency-gradient hypothesis. Limnol. Oceanogr. 53, 2374–2382 (2008).ADS 
    Article 

    Google Scholar 
    30.Bergström, A.-K., Karlsson, J., Karlsson, D. & Vrede, T. Contrasting plankton stoichiometry and nutrient regeneration in northern arctic and boreal lakes. Aquat. Sci. https://doi.org/10.1007/s00027-018-0575-2 (2018).Article 

    Google Scholar 
    31.Sterner, R. W. On the phosphorus limitation paradigm for lakes. Int. Rev. Hydrobiol. 93, 433–445. https://doi.org/10.1002/iroh.200811068 (2008).CAS 
    Article 

    Google Scholar 
    32.Sterner, R. W. C: N: P stoichiometry in Lake superior: Freshwater sea as end member. Inland Waters 1, 29–46 (2011).CAS 
    Article 

    Google Scholar 
    33.Modenutti, B. E. et al. Environmental changes affecting light climate in oligotrophic mountain lakes: The deep chlorophyll maxima as a sensitive variable. Aquat. Sci. 75, 361–371. https://doi.org/10.1007/s00027-012-0282-3 (2013).CAS 
    Article 

    Google Scholar 
    34.Longhi, M. L. & Beisner, B. E. Environmental factors controlling the vertical distribution of phytoplankton in lakes. J. Plankton Res. 31, 1195–1207. https://doi.org/10.1093/plankt/fbp065 (2009).CAS 
    Article 

    Google Scholar 
    35.Leach, T. H. et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: The relative importance of light and thermal stratification. Limnol. Oceanogr. 63, 628–646. https://doi.org/10.1002/lno.10656 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Laspoumaderes, C. et al. Glacier melting and stoichiometric implications for lake community structure: Zooplankton species distributions across a natural light gradient. Glob. Change Biol. 19, 316–326. https://doi.org/10.1111/gcb.12040 (2013).ADS 
    Article 

    Google Scholar 
    37.Jacobs, A. F. G., Jetten, T. H., Lucassen, D., Heusinkveld, B. G. & Joost, P. N. Diurnal temperature fluctuations in a natural shallow water body. Agric. For. Meteorol. 88, 269–277. https://doi.org/10.1016/S0168-1923(97)00039-7 (1997).ADS 
    Article 

    Google Scholar 
    38.Vilas, M. P., Marti, C. L., Adams, M. P., Oldham, C. E. & Hipsey, M. R. Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: A proposed feedback mechanism of macrophyte loss. Front. Plant Sci. 8, 2097. https://doi.org/10.3389/fpls.2017.02097 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Burks, R. L., Lodge, D. M., Jeppesen, E. & Lauridsen, T. L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshwat. Biol. 47, 343–365 (2002).Article 

    Google Scholar 
    40.Morris, D. P. et al. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40, 1381–1391 (1995).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Balseiro, E. G., Modenutti, B. E., Queimaliños, C. & Reissig, M. Daphnia distribution in Andean Patagonian lakes: Effect of low food quality and fish predation. Aquat. Ecol. 41, 599–609 (2007).CAS 
    Article 

    Google Scholar 
    42.Modenutti, B. E., Wolinski, L., Souza, M. S. & Balseiro, E. G. When eating a prey is risky: Implications for predator diel vertical migration. Limnol. Oceanogr. 63, 939–950. https://doi.org/10.1002/lno.10681 (2018).ADS 
    Article 

    Google Scholar 
    43.Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73. https://doi.org/10.1038/417070a (2002).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Acharya, K., Kyle, M. & Elser, J. J. Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnol. Oceanogr. 49, 656–665 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Souza, M. S., Hansson, L.-A., Hylander, S., Modenutti, B. E. & Balseiro, E. G. Rapid enzymatic response to compensate UV radiation in copepods. PLoS ONE 7, e32046. https://doi.org/10.1371/journal.pone.0032046 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Wolinski, L., Modenutti, B., Souza, M. S. & Balseiro, E. Interactive effects of temperature, ultraviolet radiation and food quality on zooplankton alkaline phosphatase activity. Environ. Pollut. 213, 135–142. https://doi.org/10.1016/j.envpol.2016.02.016 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Xie, J. et al. Physiological effects of compensatory growth during the larval stage of the ladybird Cryptolaemus montrouzieri. J. Insect Physiol. 83, 37–42. https://doi.org/10.1016/j.jinsphys.2015.11.001 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Dmitriew, C. & Rowe, L. Resource limitation, predation risk and compensatory growth in a damselfly. Oecologia 142, 150–154. https://doi.org/10.1007/s00442-004-1712-2 (2005).ADS 
    Article 
    PubMed 

    Google Scholar 
    49.Malzahn, A. M. & Boersma, M. Effects of poor food quality on copepod growth are dose dependent and non-reversible. Oikos 121, 1408–1416. https://doi.org/10.1111/j.1600-0706.2011.20186.x (2012).Article 

    Google Scholar 
    50.Droop, M. R. Some thoughts on nutrient limitation in algae. J. PhycoI. 9, 264–272 (1973).CAS 
    Article 

    Google Scholar 
    51.Boersma, M. The nutritional quality of P-limited algae for Daphnia. Limnol. Oceanogr. 45, 1157–1161 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    52.Plath, K. & Boersma, M. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 82, 1260–1269 (2001).Article 

    Google Scholar 
    53.Barbiero, R. P. & Tuchman, M. L. Results from the US EPA’s biological open water surveillance program of the Laurentian Great Lakes: II. Deep chlorophyll maxima. J. Great Lakes Res. 27, 155–166 (2001).CAS 
    Article 

    Google Scholar 
    54.Camacho, A. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica 25, 453–478 (2006).
    Google Scholar 
    55.Pérez, G. L., Queimaliños, C. P. & Modenutti, B. E. Light climate and plankton in the deep chlorophyll maxima in North Patagonian Andean lakes. J. Plankton Res. 24, 591–599 (2002).Article 

    Google Scholar 
    56.Magee, M. R. & Wu, C. H. Response of water temperatures and stratification to changing climate in three lakes with different morphometry. Hydrol. Earth Syst. Sci. 21, 6253–6274. https://doi.org/10.5194/hess-21-6253-2017 (2017).ADS 
    Article 

    Google Scholar 
    57.Niedrist, G. H., Psenner, R. & Sommaruga, R. Climate warming increases vertical and seasonal water temperature differences and inter-annual variability in a mountain lake. Clim. Change 151, 473–490. https://doi.org/10.1007/s10584-018-2328-6 (2018).ADS 
    Article 

    Google Scholar 
    58.Kilham, S. S., Kreeger, D. A., Lynn, S. G., Goulden, C. E. & Herrera, L. COMBO – A defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377, 147–159 (1998).CAS 
    Article 

    Google Scholar 
    59.Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide c. J. Phycol. 8, 10–14 (1972).CAS 

    Google Scholar 
    60.Balseiro, E. G., Souza, M. S., Modenutti, B. E. & Reissig, M. Living in transparent lakes: Low food P: C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnol. Oceanogr. 53, 2383–2390 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    61.Laspoumaderes, C., Souza, M. S., Modenutti, B. E. & Balseiro, E. Glacier melting and response of Daphnia oxidative stress. J. Plankton Res. 39, 675–686. https://doi.org/10.1093/plankt/fbx028 (2017).CAS 
    Article 

    Google Scholar 
    62.APHA. Standard methods for the examination of water and wastewater. (American Public Health Association, AWWA, 2005).63.Gorokhova, E. & Kyle, M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J. Plankton Res. 24, 511–522 (2002).CAS 
    Article 

    Google Scholar  More