More stories

  • in

    The influence of different morphological units on the turbulent flow characteristics in step-pool mountain streams

    Step-pools are natural geomorphologic forms developed under the action of extreme floods1 in mountain streams with bed slopes ranging from 3 to 20%2,3. The step-pools are characterized by poorly graded bed materials intricately packed to form a step and pool sequence, generating high energy tumbling and tranquil mountain flows. The typical bed morphology is irregular and results in spatially and temporally varied hydrodynamics over various functional units within the step-pools such as step, tread, base of step, and pool region (Fig. 1b). The step denotes the portion of bed comprising boulders or bedrock outcrops jam-packed across the width of the channel. The pool consists of finer bed materials and deeper cross-sections as a result of scour due to submerged or unsubmerged hydraulic jumps generated in the pool. The base of step is the section immediately downstream of step unit where the flow over the step impinges into the pool with high amounts of turbulence and self-aeration. The tread is the region extending from the downstream end of the scour pool up to the step unit. Step-pool systems can also exist without the presence of a tread region. In that case, the pool region directly ends in a step unit4.Figure 1Details of step-pool systems in the present study: (a) Longitudinal section of the field site, (b) Longitudinal section of the laboratory model, (c) Photograph of the field site, (d) Photograph of the experimental setup.Full size imageThe evaluation of flow parameters in step-pool streams does not follow the general criteria recommended for lowland rivers. The commonly used flow friction factors such as Manning’s n and Chezy’s C cannot be applied here due to the non-uniform nature of flow at meso-scale. In step-pool mountain streams, the rational frictional coefficient to define flow resistance is the non-dimensional Darcy Weisbach friction factor5,6,7. Dedicated field and laboratory investigations of the step-pools are necessary to create a sufficient database for the development of accurate hydraulic models.In addition, the design of step-pools is adopted for stream restorations8,9, storm water conveyance systems10, and for creating close-to-nature step-pool fish passes11,12,13. Primal research on step-pools has been largely limited to the analysis of bed morphology14,15,16,17, flow resistance18,19,20,21,22 and sediment transport23,24 by considering the step-pool reach as a single system. A detailed review on the hydrodynamics of step-pools in mountain streams is available in Kalathil and Chandra7.The variations in the flow characteristics imposed by the various morphological units within the step-pool system (SPS) were not studied until the 2000s. Adverse pressure gradients in the pools and upstream of steps lead to increased turbulence, while favourable pressure gradients on steps suppress turbulence. Accordingly, pools are dominated by wake turbulence and the steps, treads and runs are governed by form or bed-generated turbulence. The wake turbulence in pools is characterized by recirculation eddies and its strength diminishes with increase in distance from the impingement point25,26. Incidentally, the variations in hydrodynamics within step-pool systems do not furnish considerable differences in the sediment transport estimation since the measured and computed magnitudes differ up to an order of three because of the limited sediment availability in mountain streams27,28. Nevertheless, updated knowledge on the flow dynamics at different regions within the step-pool reach will aid in providing guidelines for designing close-to-nature fish passes to enable target species to pass through the fluvial system29,30. In recent times, with increased demands to implement and maintain environmental flow schemes, cost-effective and eco-friendly structures such as step-pools provide a promising tool to facilitate economic development together with ecological conservation.The presence of a wide range of substrates (fine sand to boulders) and varying flow conditions in step-pools facilitate the inhabitation, migration, and dispersal of diverse aquatic species31. The productive range of water depth and flow velocity for inhabitation lies between 0.16 m to 0.5 m and 0.3 m/s to 1.2 m/s, respectively11. In addition to the range of flow depth and velocity requirements, hydraulic shear stress and turbulence characteristics also affect fish behaviour and locomotion32. Depending on the turbulence scale and intensities, various damages on the fish body or disorientation of the species may occur. Therefore, it is important to consider fish behaviour, life stage, swimming ability, and hydraulic conditions including velocity and turbulence characteristics in step-pool structures prior to its ecological applications. Adequate design guidelines for the construction of close to nature fish passes are not available due to lack of studies31,33.Limited research addresses the influence of bed morphology on the turbulence characteristics in step-pools. Wohl and Thompson4 studied the variations in flow profiles at different locations in a step-pool with the use of an electromagnetic current meter of sampling frequency 0.5 Hz. The study was limited to the analysis of mean velocity and coefficient of variation in velocity which is sometimes used synonymous to turbulence intensities. Although flow profiles showed variations in pattern, ANOVA and ANCOVA results were rather inconclusive regarding the dependence of flow parameters on the bed form types. Later on, Wilcox and Wohl34 and Wilcox et al.35 conducted three-dimensional velocity measurements using SonTek FlowTracker operating at 1 Hz sampling frequency to study the spatial variation of velocity and turbulence intensities in step-pools. The pools exhibit increased levels of turbulence intensities and less velocity reduction in cases where the upstream step-units do not span the entire width of the channel and effects as leaky or porous steps35. The turbulence characteristics in terms of the root mean square of the fluctuating velocities showed considerable differences between step, tread and pool. However, due to the low sampling frequency of the velocity measuring instrument, the accuracy of turbulence analysis is questionable. Considering the complex terrain in step-pool streams and practical difficulties in the use of high frequency instruments that require proper stationing and continuous power supply, it is arduous to produce good quality data of the fluctuating velocities. To bridge the gap in research on the fluctuating velocity components in step-pools, extensive laboratory studies are required.In this context, to shed light upon the variation of hydraulic parameters with the morphological units, we discuss the results from a physical model downscaled according to field measurements conducted in a step-pool stream in Erumakolli, Wayanad, India. Figure 1 shows the longitudinal sections and photographs of the field site and the laboratory experimental setup. The field investigation comprised the measurements of bed material size, bed topography and flow velocity measurements. The physical model study discusses the variation in the turbulence characteristics across steps, treads and pools. The analysis is limited to the vertical distribution of velocity magnitude and turbulence intensities across the morphological units, the propagation of velocity magnitude and Reynolds shear stress in the flow direction, relationship between the turbulent kinetic energy and velocity magnitude, and the evaluation of energy dissipation factor in the step-pools. The present study is the foremost attempt in the analysis and discussions of turbulence fluctuations, Reynolds shear stresses and energy dissipations in self-formed step-pool systems.Experimental setup validationThe laboratory experimental setup was created by establishing dynamic similarity between the field and the laboratory model through Froude’s Model Law. Model scales less than 10:1 can successfully simulate field conditions in the case of turbulent self-aerated flows36. A length scale ratio of 3.3: 1 was chosen for creating the physical model. The corresponding velocity scale and discharge scale are (3.3)1/2: 1 and (3.3)5/2: 1, respectively. The laboratory step-pool system is self-formed under a formative discharge and is not expected to generate the exact bed topography as observed in the field. However, effect of the influencing parameters such as D84, step-height, bed slope, and discharge on the velocity and turbulence characteristics would be adequately simulated. A comparison of the thalweg velocity and Froude number over step, tread and pool at d = 0.6 H between the field and laboratory data is presented in Table 1, where d is the depth of measurement and H is the total flow depth at that point. Since the measured data is location specific and due to the limitations in the number of data points available, only the reach scale average values of velocity and Froude number was used to estimate the error. An absolute error of 0.04 m/s (6.3%) and 0.02 (4.9%) was observed between the field and laboratory up scaled data for thalweg reach average velocity and Froude number, respectively.Table 1 Comparison of the thalweg velocity and Froude number for step, tread and pool at d = 0.6 H between the field and laboratory data.Full size tableVelocity and turbulence intensitiesThe velocity and turbulence characteristics pertinent to accurate design and model development of step-pools are velocity magnitude (VR), turbulence intensities (TI), normalized turbulent kinetic energy (K), and energy dissipation factor (EDF). We obtained velocity data in the physical model using Nortek Vectrino 3-D Acoustic Doppler Velocimeter. A total of 16 thalweg velocity data at d = 0.6H and 24 vertical velocity profiles at 1 cm intervals have been retained after velocity filtering and processing (see “Methods”), where d is the depth of measurement and H is the total flow depth at that point. The velocity measurements were confined in the range of 0.003 m/s to 0.796 m/s, bounding the productive range for aquatic species inhabitation in field scale (0.005 m/s to 1.446 m/s).The propagation of flow in a step-pool system is illustrated in Fig. 2. The x-axis shows the measurement sections along the longitudinal direction (X) for step-pool system 2 (see “Methods”). The variable on the y-axis z + H − d denotes the elevation of the measurement point above the datum which is set at the deepest scour point of X = 2.60 m. Where, z is the vertical distance from the datum to the bed surface, H is the total flow depth at the point, and d is the depth of measurement with respect to the free surface. The first vertical corresponding to X = 2.40 m is at a distance of 0.15 m downstream of a step unit. Any data collected closer to the steps were removed in data filtration. The average velocity at d = 0.6H is shown in the plot legend. The lowest velocity is observed at the deepest scour section of X = 2.60 m.Figure 2Variation of resultant velocity magnitude VR in the longitudinal direction of the SPS 2.Full size imageTo examine the statistical differences in the distribution of velocity and turbulence intensities across the morphological units, the 24 vertical velocity measurements comprising longitudinal and cross-stream points have been subjected to Kruskal–Wallis ANOVA. The earlier studies that sought to distinguish the morphological units on the basis of velocity components performed one-way ANOVA on the datasets. Although the measurements on steps, treads and pools are independent of each other and randomly sampled, the available data fails to uniformly conform to normal distribution, which is a prerequisite for ANOVA test. Therefore, the present work revisits this analysis for velocity components, velocity magnitude and turbulence intensities using Kruskal–Wallis ANOVA which is a non-parametric test that does not assume a normally distributed dataset. The analysis is conducted on the ranks of the data values rather than the data values, and tests whether the median values are significantly different from each other. A resultant p value of 0 from the analysis indicates that there is significant difference between the groups, while a p value of 1 indicates vice-versa. The null hypothesis of Kruskal–Wallis ANOVA is that the sample groups come from the same population. Closeness of the p value to 0 is a measure of the confidence in rejecting the null hypothesis. In the present study, data points were categorized with respect to d/H values to normalize the effect of depth on the velocity variations, and the data points confined in the range d/H = 0.50–0.70 were considered for the test (Case I). The d/H is thus selected to obtain a wider range of data points pertaining to the average velocity which is typically at d/H = 0.6. The non-parametric test was also repeated for depth averaged values (Case II) to produce similar results. Except in the case of cross-stream velocity v, all other groupings showed significant difference between the median values for step, tread and pool data points. The p values of 0.24 and 0.41 were obtained for the hypothesis test on v for Case I and Case II, respectively. This shows that the variation in the cross-stream velocity is independent of the morphological type and is not a characteristic feature of step-pool system in a straight channel. The step-pool system that encounters bends within the reach may have an influence on the cross-stream velocity component. The results of the statistical analysis and box-plots of the velocity magnitude and turbulence intensities for both Cases I and II are given in Table 2 and Fig. 3, respectively. A negligible absolute error of 0.027 m/s and 0.031 m/s in velocity magnitude was obtained between the mean and median of Cases I and II, respectively. Whereas, a maximum absolute error of 0.134 and 0.087 was observed in the respective turbulence intensities. However, the differences in the methods are not substantial enough to alter the results of the hypothesis testing.Table 2 Comparison and analysis results of Kruskal–Wallis ANOVA for data points in the range of d/H = 0.50–0.70 and depth-averaged values at various verticals across the morphological units.Full size tableFigure 3Distribution of resultant velocity magnitude VR and turbulence intensities TI of the fluctuating velocities, u′, v′, and w′ for different morphological unit: (a) Case I: data points confined to d/H = 0.50–0.70. (b) Case II: depth-averaged values at each vertical.Full size imageThe average values of TIu′, TIv′, and TIw′ combining the 24 verticals (d/H ranging from 0.20 to 1.00) are 0.065,0.055 and 0.097 for steps, 0.146, 0.110, and 0.165 for treads, and 0.453, 0.265, and 0.523 for pools, respectively. The values show an increase of 55%, 50% and 41% for TIv′ with respect to TIu′ for step, tread and pool, respectively, while a sizeable increase of 597%, 382% and 439% for TIw′ with respect to TIu′, which evidently indicates the dominance of vertical fluctuations in the pools. The pattern of variation of turbulence intensities at step, tread and pools can be better understood with the help of vertical profiles. Figure 4 shows the vertical profiles of velocity magnitude and turbulence intensity profiles corresponding to step, tread and pool regions in different step-pool systems, namely, SPS 1, SPS 2, and SPS 3 (see “Methods”). Compared to the velocity profiles in step and tread, a visible mid-profile shear layer can be seen in the pool. Previous researchers have identified the presence of mid-profile shear in regions of wake turbulence. Thompson and Wohl4 illustrated the shear layer downstream of steps with the help of velocity profiles in step-pool systems. Baki et al.37 illustrated the presence of shear layer in the wake turbulence regions of a rock-ramp fish pass. A staggered arrangement of natural boulders of equivalent diameter 14 cm was used to prepare the rock-ramp bed. The wake area downstream of the boulders is similar to the downstream of steps in step-pool systems. Fang et al.38 illustrated the shift in the vertical profile of Reynolds shear stress due to near-bed and boulder-induced shear stresses. In the present study, the shear layer is prominent in SPS 3, milder in SPS 1 and fairly non-existent in SPS 2 which corresponds to the profile at X = 2.40 m in Fig. 2. The shear layer is generated due to the momentum exchange occurring in the pools consequent to flow impingement. The occurrence of the shear layer and the magnitude of velocity shift depend on the characteristics of the upstream step unit and spacing between the upstream step and point of interest. In the case of leaky step units where some portion of the step cross section is devoid of elevated step units, the flow passes through without causing consideration impingement to the downstream pool. Hence, the flow does not produce a downstream wake region resulting in the absence of shear layers in the vertical profile. The same can be observed from Fig. 4e, where the vertical section in SPS 2 existed downstream of a leaky step unit, which also lead to lower levels of energy dissipation and less velocity reduction.Figure 4Variation of resultant velocity magnitude VR and turbulence intensities TI of the fluctuating velocities, u′, v′, and w′ along the depth: (a) VR at Step, (b) TI at Step, (c) VR at Tread, (d) TI at Tread, (e) VR at Pool, and (f) TI at Pool.Full size imageThe magnitude of turbulence intensities is lower on step and tread, and maximum in the pools as can be observed in Fig. 4b, d and f, respectively. The fluctuations are higher in the pools due to the varied velocity distribution and wake turbulence characteristics in the pools.Reynolds shear stressReynolds shear stress is the stress generated due to the momentum exchange between the fluctuating velocity components. The range of shear stress in the flow medium has implications in the suitability of a flow body to various aquatic lives since high levels of shear stress may even lead to major injuries or mortality to the species. The vertical profiles of the time averaged and normalized Reynolds shear stress in the x–z plane in the longitudinal direction is shown in Fig. 5. The x-axis shows the normalized Reynolds shear stress (- overline{{u^{{prime }} w^{{prime }} }} /V_{max }^{2}) for each section, where Vmax = 0.796 m/s is the maximum velocity measured during the experimental runs. The variable on the y-axis follows the same convention as described in Fig. 2. The fluctuations in the profile are more in the deeper locations in the pool (X = 2.40 m to 2.80 m) due to the increased turbulence at the bottom as a result of flow impingement. The error bar shown for X = 2.50, 2.90 and 3.05 is calculated from the additional 4 verticals measured in the cross-stream direction, for each of the sections. The maximum Reynolds shear stress variation is observed in x–z plane compared to x–y and y–z planes, with normalized values ranging from − 19.477 to 13.729. The absolute maximum value of 19.477 amounts to 12.34 N/m2 in model scale and 40.73 N/m2 in prototype scale. Reynolds shear stress as low as 30 N/m2 can cause reduction in startle response in some species39. Therefore, ensuring acceptable limits of turbulence fluctuations is essential in the design for artificial constructions of the step-pool morphology. While recreating the morphology for a fish pass design, control can be placed on the pool volume, characteristic grain size (equivalent to step height) or allowable discharge to reduce the turbulence levels in pools. However, this entails detailed study into the cause and effect of these parameters on the hydrodynamics.Figure 5Variation of time averaged and normalized Reynolds shear stress in the x–z plane (( – overline{{u^{{prime }} w^{{prime }} }} /V_{max }^{2} )) in the longitudinal direction of SPS 2 (Vmax = 0.796 m/s).Full size imageTurbulent kinetic energyAnother indicator of turbulence characteristic to the morphological units in the present study is Turbulent Kinetic Energy (TKE) which is a measure of kinetic energy per unit mass of the turbulent flow. It is an important parameter that determines the locomotive characteristics of various species40 and key to evaluating the energy loss to fishes41. In the present study, normalized form of turbulent kinetic energy (K) follows an inverse power relation to the velocity magnitude as shown in Fig. 6. The x-axis is normalized using Vmax and TKE is normalized by the transformation (K = sqrt {{text{TKE}}} /V_{R}). The data is inclusive of all the depth-wise data points measured over step, tread and pool regions along the thalweg. Larger values of K occurred in pools followed by tread and step regions. The pattern is comprehensible from visual observation of the flow field, where the flow occurs as high-velocity sheet with limited agitation over tread and step, resulting in plunging flow with recirculating eddies in the pools. A non-linear curve fitting of type Power-Allometric 1 was used to generate the empirical equation (K = aleft( {{{V_{R} } mathord{left/ {vphantom {{V_{R} } {V_{max } }}} right. kern-nulldelimiterspace} {V_{max } }}} right)^{b}), where a = 0.12398 and b = − 0.89947 with a standard error of ± 0.01018 and ± 0.03398, respectively. The coefficient of determination of the plot is 0.93.Figure 6Variation of normalized turbulent kinetic energy K with the time-averaged thalweg velocity ratio VR/Vmax (Vmax = 0.796 m/s).Full size imageEnergy dissipation factorThe energy dissipation factor (EDF) is an engineering design parameter that checks the turbulence level in the fish pathways. The flow energy must be sufficiently dissipated to ensure velocity levels less than 2 m/s. The EDF is also representative of the eddies and turbulence generated due to flow impingement into pools. Contrary to the conventional pool fish passes and slot fish passes, the pool cross-sections in natural step-pools are not uniform33. The pool dimensions vary along the reach and accordingly reflects in the EDF values. Hence, calculation of EDF using the equation (EDF=gamma QS/A) would result in considerable errors since A is not a constant within and across step-pool systems, where γ is the specific weight of water, Q is the discharge, S is the bed slope and A is the cross-sectional area of the pool. Here, the EDF calculations were based on the basic equation (EDF = gamma QDelta H/forall), where ΔH is the drop in water elevation level per pool and (forall) is the pool volume. The step-pool systems 1, 2 and 3 have been evaluated for EDF. The pool volume was calculated applying the trapezoidal rule to the wetted areas of cross-sections in pool spaced at 10 cm apart. The wetted area was calculated from the measured bed and water elevation levels. The region starting immediately downstream of the steps up to the exit slope of the scour pool is considered for calculating the pool volume. Table 3 presents the pool dimensions and EDF values obtained in the present study. The EDF values obtained for step-pool systems 1, 2, and 3 were 321, 207, and 123 W/m3 in model scale, respectively. The results corresponds to 590, 380, and 226 W/m3 in prototype scale. However, a value of 150 W/m3 should not be exceeded to ensure acceptable levels of turbulence in the pools33. Specific EDF criteria for various fish species are available to design fish passes accommodating the requirements of the predominant fish population42.Table 3 Computation of energy dissipation factor in step-pool systems 1, 2 and 3.Full size tableConsidering the range of shear stresses and energy dissipation factors obtained in the present study, it can be inferred that construction of step-pool fish passes simulating the field parameters may not provide adequate flow conditions for a step-pool type fish pass. For the design of step-pool type fish passes, the pool volumes should be back calculated from the EDF equation for specific species. The translation of the pool volume in terms of the width of channel, pool length and pool depth will ensure lower levels of turbulence intensities and shear stresses in the passage. Since the interest towards close-to nature fish passes have been developed only in the recent years, specific guidelines for step-pool type fish passes are yet to be formulated. This calls for research in artificial step-pool constructions based on the pool and turbulence requirements of the dominant target species. Nevertheless, the nature of hydrodynamics in the self-formed and artificially constructed would coincide since the step-pool bed morphology has an inherent tendency to attain a state of maximum resistance. The concept of creating artificial structures is limited to providing and placing the bed materials into required bed slopes and approximate design dimensions. The ultimate bed morphology of the structure will be modelled over time by the hydraulic force of the flowing water. More

  • in

    Inter-species interactions alter antibiotic efficacy in bacterial communities

    1.Filkins LM, O’Toole GA. Cystic fibrosis lung infections: polymicrobial, complex, and hard to treat. PLoS Pathog. 2015;11:e1005258.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    2.Paterson IK, Hoyle A, Ochoa G, Baker-Austin C, Taylor NGH. Optimising antibiotic usage to treat bacterial infections. Sci Rep. 2016;6:37853.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Andrews JM. Determination of minimum inhibitory concentrations. J Antimicrob Chemother. 2001;48:5–16.CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Brook I. Inoculum effect. Rev Infect Dis. 1989;11:361–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Karslake J, Maltas J, Brumm P, Wood KB. Population density modulates drug inhibition and gives rise to potential bistability of treatment outcomes for bacterial infections. PLOS Comput Biol. 2016;12:e1005098.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    6.Udekwu KI, Parrish N, Ankomah P, Baquero F, Levin BR. Functional relationship between bacterial cell density and the efficacy of antibiotics. J Antimicrob Chemother. 2009;63:745–57.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Sweeney E, Sabnis A, Edwards AM, Harrison F. Effect of host-mimicking medium and biofilm growth on the ability of colistin to kill Pseudomonas aeruginosa. Microbiology. 2020;166:1171–80.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Walters MC, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother. 2003;47:317–23.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science. 2011;334:982–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35:322–32.PubMed 
    Article 
    CAS 

    Google Scholar 
    11.Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis. 2015;34:877–86.CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Macia MD, Rojo-Molinero E, Oliver A. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin Microbiol Infect. 2014;20:981–90.CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Thieme L, Hartung A, Tramm K, Klinger-Strobel M, Jandt KD, Makarewicz O, et al. MBEC versus MBIC: the lack of differentiation between biofilm reducing and inhibitory effects as a current problem in biofilm methodology. Biol Proced Online. 2019;21:18.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    14.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 
    15.Smith AL, Fiel SB, Mayer-Hamblett N, Ramsey B, Burns JL. Susceptibility testing of Pseudomonas aeruginosa isolates and clinical response to parenteral antibiotic administration: lack of association in cystic fibrosis. Chest. 2003;123:1495–502.CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Radlinski L, Conlon B. Antibiotic efficacy in the complex infection environment. Curr Opin MicrobioL 2018;42:19–24.CAS 
    PubMed 
    Article 

    Google Scholar 
    17.Vos MGJ, de, Zagorski M, McNally A, Bollenbach T. Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections. PNAS. 2017;114:10666–71.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    18.Adamowicz EM, Flynn J, Hunter RC, Harcombe WR. Cross-feeding modulates antibiotic tolerance in bacterial communities. ISME J. 2018;12:2723–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Aranda-Díaz A, Obadia B, Dodge R, Thomsen T, Hallberg ZF, Güvener ZT, et al. Bacterial interspecies interactions modulate pH-mediated antibiotic tolerance. eLife. 2020;9:e51493.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Vega NM, Gore J. Collective antibiotic resistance: mechanisms and implications. Curr Opin Microbiol. 2014;21:28–34.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Beaudoin T, Yau YCW, Stapleton PJ, Gong Y, Wang PW, Guttman DS, et al. Staphylococcus aureus interaction with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. NPJ Biofilms Microbiomes. 2017;3:25.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Orazi G, O’Toole GA. Pseudomonas aeruginosa alters Staphylococcus aureus sensitivity to vancomycin in a biofilm model of cystic fibrosis infection. mBio. 2017;8:e00873–17.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Sorg RA, Lin L, Doorn GS, van, Sorg M, Olson J, Nizet V, et al. Collective resistance in microbial communities by intracellular antibiotic deactivation. PLOS Biol. 2016;14:e2000631.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    24.Perlin MH, Clark DR, McKenzie C, Patel H, Jackson N, Kormanik C, et al. Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations. Proc R Soc B. 2009;276:3759–68.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Flynn JM, Cameron LC, Wiggen TD, Dunitz JM, Harcombe WR, Hunter RC. Disruption of cross-feeding inhibits pathogen growth in the sputa of patients with cystic fibrosis. mSphere. 2020;5:e00343–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Gurney J, Brown SP, Kaltz O, Hochberg ME. Steering phages to combat bacterial pathogens. Trends Microbiol. 2020;28:85–94.CAS 
    PubMed 
    Article 

    Google Scholar 
    27.Waters VJ, Kidd TJ, Canton R, Ekkelenkamp MB, Johansen HK, LiPuma JJ, et al. Reconciling antimicrobial susceptibility testing and clinical response in antimicrobial treatment of chronic cystic fibrosis lung infections. Clin Infect Dis. 2019;69:1812–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Somayaji R, Parkins MD, Shah A, Martiniano SL, Tunney MM, Kahle JS, et al. Antimicrobial susceptibility testing (AST) and associated clinical outcomes in individuals with cystic fibrosis: a systematic review. J Cyst Fibros. 2019;18:236–43.CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Raghuvanshi R, Vasco K, Vázquez-Baeza Y, Jiang L, Morton JT, Li D, et al. High-resolution longitudinal dynamics of the cystic fibrosis sputum microbiome and metabolome through antibiotic therapy. mSystems. 2020;5:e00292–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    30.Cystic Fibrosis Trust. UK cystic fibrosis registry annual data report 2019. 2020. [online] Available at: https://www.cysticfibrosis.org.uk/sites/default/files/2020-12/2019%20Registry%20Annual%20Data%20report_Sep%202020.pdf [Accessed 5 June 2021].31.Nixon GM, Armstrong DS, Carzino R, Carlin JB, Olinsky A, Robertson CF, et al. Clinical outcome after early Pseudomonas aeruginosa infection in cystic fibrosis. J Pediatr. 2001;138:699–704.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Sánchez MB. Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol. 2015;6:658.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Salsgiver EL, Fink AK, Knapp EA, LiPuma JJ, Olivier KN, Marshall BC, et al. Changing epidemiology of the respiratory bacteriology of patients with cystic fibrosis. Chest. 2016;149:390–400.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Cystic Fibrosis Trust. Antibiotic treatment for cystic fibrosis. 2009. [online] Available at: https://www.cysticfibrosis.org.uk/sites/default/files/2020-11/Anitbiotic%20Treatment.pdf [Accessed 7 June 2021].35.Denton M, Todd NJ, Littlewood JM. Role of anti-pseudomonal antibiotics in the emergence of Stenotrophomonas maltophilia in cystic fibrosis patients. Eur J Clin Microbiol Infect Dis. 1996;15:402–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Esposito A, Pompilio A, Bettua C, Crocetta V, Giacobazzi E, Fiscarelli E, et al. Evolution of Stenotrophomonas maltophilia in cystic fibrosis lung over chronic infection: a genomic and phenotypic population study. Front Microbiol. 2017;8:1590.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Pompilio A, Crocetta V, De Nicola S, Verginelli F, Fiscarelli E, Di Bonaventura G. Cooperative pathogenicity in cystic fibrosis: Stenotrophomonas maltophilia modulates Pseudomonas aeruginosa virulence in mixed biofilm. Front Microbiol. 2015;6:951.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Dalbøge CS, Hansen CR, Pressler T, Høiby N, Johansen HK. Chronic pulmonary infection with Stenotrophomonas maltophilia and lung function in patients with cystic fibrosis. J Cyst Fibros. 2011;10:318–25.PubMed 
    Article 

    Google Scholar 
    39.Okazaki A, Avison MB. Induction of L1 and L2 β-lactamase production in Stenotrophomonas maltophilia is dependent on an AmpR-type regulator. Antimicrob Agents Chemother. 2008;52:1525–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Yurtsev EA, Chao HX, Datta MS, Artemova T, Gore J. Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol Syst Biol. 2013;9:683.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Bottery MJ, Wood AJ, Brockhurst MA. Selective conditions for a multidrug resistance plasmid depend on the sociality of antibiotic resistance. Antimicrob Agents Chemother. 2016;60:2524–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Palmer KL, Aye LM, Whiteley M. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol. 2007;189:8079–87.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Artemova T, Gerardin Y, Dudley C, Vega NM, Gore J. Isolated cell behavior drives the evolution of antibiotic resistance. Mol Syst Biol. 2015;11:822.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    44.Harrison E, Wood AJ, Dytham C, Pitchford JW, Truman J, Spiers A, et al. Bacteriophages limit the existence conditions for conjugative plasmids. mBio. 2015;6:e00586–15.PubMed 
    PubMed Central 

    Google Scholar 
    45.Hall JPJ, Wood AJ, Harrison E, Brockhurst MA. Source–sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities. PNAS. 2016;113:8260–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Regoes RR, Wiuff C, Zappala RM, Garner KN, Baquero F, Levin BR. Pharmacodynamic functions: a multiparameter approach to the design of antibiotic treatment regimens. Antimicrob Agents Chemother. 2004;48:3670–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Yu G, Baeder DY, Regoes RR, Rolff J. Predicting drug resistance evolution: insights from antimicrobial peptides and antibiotics. Proc R Soc B. 2018;285:20172687.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Zhanel GG, Simor AE, Vercaigne L, Mandell L. Imipenem and meropenem: comparison of in vitro activity, pharmacokinetics, clinical trials and adverse effects. Can J Infect Dis. 1998;9:215–28.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    49.Gould VC, Okazaki A, Avison MB. β-Lactam resistance and β-lactamase expression in clinical Stenotrophomonas maltophilia isolates having defined phylogenetic relationships. J Antimicrob Chemother. 2006;57:199–203.CAS 
    PubMed 
    Article 

    Google Scholar 
    50.European Cystic Fibrosis Society Patient Registry. ECFS patient registry annual data report 2018. 2020. [online] Available at: https://www.ecfs.eu/sites/default/files/general-content-files/working-groups/ecfs-patient-registry/ECFSPR_Report_2018_v1.4.pdf [Accessed 7 June 2021].51.Radlinski L, Rowe SE, Kartchner LB, Maile R, Cairns BA, Vitko NP, et al. Pseudomonas aeruginosa exoproducts determine antibiotic efficacy against Staphylococcus aureus. PLoS Biol. 2017;15:e2003981.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    52.Harrison FY. Microbial ecology of the cystic fibrosis lung. Microbiology. 2007;153:917–23.CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Keel RA, Sutherland CA, Crandon JL, Nicolau DP. Stability of doripenem, imipenem and meropenem at elevated room temperatures. Int J Antimicrob Agents. 2011;37:184–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Okazaki A, Avison MB. Aph(3′)-IIc, an Aminoglycoside resistance determinant from Stenotrophomonas maltophilia. Antimicrob Agents Chemother. 2007;51:359–60.CAS 
    PubMed 
    Article 

    Google Scholar 
    55.Li X-Z, Zhang L, McKay GA, Poole K. Role of the acetyltransferase AAC(6′)-Iz modifying enzyme in aminoglycoside resistance in Stenotrophomonas maltophilia. J Antimicrob Chemother. 2003;51:803–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    56.Frost I, Smith WPJ, Mitri S, Millan AS, Davit Y, Osborne JM, et al. Cooperation, competition and antibiotic resistance in bacterial colonies. ISME J. 2018;12:1582–93.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Yin C, Yang W, Meng J, Lv Y, Wang J, Huang B. Co-infection of Pseudomonas aeruginosa and Stenotrophomonas maltophilia in hospitalised pneumonia patients has a synergic and significant impact on clinical outcomes. Eur J Clin Microbiol Infect Dis. 2017;36:2231–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Waters V, Yau Y, Prasad S, Lu A, Atenafu E, Crandall I, et al. Stenotrophomonas maltophilia in cystic fibrosis: serologic response and effect on lung disease. Am J Respir Crit Care Med. 2011;183:635–40.PubMed 
    Article 

    Google Scholar 
    59.Goss CH, Mayer-Hamblett N, Aitken ML, Rubenfeld GD, Ramsey BW. Association between Stenotrophomonas maltophilia and lung function in cystic fibrosis. Thorax. 2004;59:955–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Mojica MF, Ouellette CP, Leber A, Becknell MB, Ardura MI, Perez F, et al. Successful treatment of bloodstream infection due to metallo-β-lactamase-producing Stenotrophomonas maltophilia in a renal transplant patient. Antimicrob Agents Chemother. 2016;60:5130–4.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.McCutcheon JG, Dennis JJ. The potential of phage therapy against the emerging opportunistic pathogen Stenotrophomonas maltophilia. Viruses. 2021;13:1057.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Rossi E, La Rosa R, Bartell JA, Marvig RL, Haagensen JAJ, Sommer LM, et al. Pseudomonas aeruginosa adaptation and evolution in patients with cystic fibrosis. Nat Rev Microbiol. 2021;19:331–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Davies EV, James CE, Brockhurst MA, Winstanley C. Evolutionary diversification of Pseudomonas aeruginosa in an artificial sputum model. BMC Microbiol. 2017;17:3.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Bara JJ, Matson Z, Remold SK. Life in the cystic fibrosis upper respiratory tract influences competitive ability of the opportunistic pathogen Pseudomonas aeruginosa. R Soc Open Sci. 2018;5:180623.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    65.Bartell JA, Sommer LM, Haagensen JAJ, Loch A, Espinosa R, Molin S, et al. Evolutionary highways to persistent bacterial infection. Nat Commun. 2019;10:629.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Estrela S, Brown SP. Community interactions and spatial structure shape selection on antibiotic resistant lineages. PLOS Comput Biol. 2018;14:e1006179.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    67.McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J, Brown SP, et al. Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat Commun. 2017;8:14371.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol. 2006;72:3916–23.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    69.Willner D, Haynes MR, Furlan M, Schmieder R, Lim YW, Rainey PB, et al. Spatial distribution of microbial communities in the cystic fibrosis lung. ISME J. 2012;6:471–4.CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Turner KH, Wessel AK, Palmer GC, Murray JL, Whiteley M. Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. PNAS. 2015;112:4110–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Kirchner S, Fothergill JL, Wright EA, James CE, Mowat E, Winstanley C. Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J Vis Exp. 2012;64:e3857.
    Google Scholar 
    72.Harrison F, Diggle SP. An ex vivo lung model to study bronchioles infected with Pseudomonas aeruginosa biofilms. Microbiology. 2016;162:1755–60.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Harrington NE, Sweeney E, Harrison F. Building a better biofilm – formation of in vivo-like biofilm structures by Pseudomonas aeruginosa in a porcine model of cystic fibrosis lung infection. Biofilm. 2020;2:100024.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Bricio-Moreno L, Sheridan VH, Goodhead I, Armstrong S, Wong JKL, Waters EM, et al. Evolutionary trade-offs associated with loss of PmrB function in host-adapted Pseudomonas aeruginosa. Nat Commun. 2018;9:2635.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    75.Castellani S, Di Gioia S, di Toma L, Conese M. Human cellular models for the investigation of lung inflammation and mucus production in cystic fibrosis. Anal Cell Pathol. 2018;2018:3839803.Article 
    CAS 

    Google Scholar 
    76.Levin-Reisman I, Ronin I, Gefen O, Braniss I, Shoresh N, Balaban NQ. Antibiotic tolerance facilitates the evolution of resistance. Science. 2017;355:826–30.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Wistrand-Yuen E, Knopp M, Hjort K, Koskiniemi S, Berg OG, Andersson DI. Evolution of high-level resistance during low-level antibiotic exposure. Nat Commun. 2018;9:1599.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    78.Choi K-H, Schweizer HP. mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc. 2006;1:153–61.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    79.Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and Its applications to single-cell Sequencing. J Comput Biol. 2012;19:455–77.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS 
    Article 

    Google Scholar 
    81.Onoue Y, Mori M. Amino acid requirements for the growth and enterotoxin production by Staphylococcus aureus in chemically defined media. Int J Food Microbiol. 1997;36:77–82.CAS 
    PubMed 
    Article 

    Google Scholar 
    82.Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Lefort V, Longueville J-E, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol. 2017;34:2422–4.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Kuznetsov A, Bollin CJ. NCBI Genome Workbench: desktop software for comparative genomics, visualization, and GenBank data submission. Methods Mol Biol. 2021;2231:261–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    86.Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Sexual dimorphism in size and shape of the head in the sea snake Emydocephalus annulatus (Hydrophiinae, Elapidae)

    1.Andersson, M. Sexual Selection (Princeton University Press, 1996).
    Google Scholar 
    2.Clutton-Brock, T. H. The Evolution of Parental Care (Princeton University Press, 1991).Book 

    Google Scholar 
    3.Olsson, M., Shine, R., Wapstra, E., Ujvari, B. & Madsen, T. Sexual dimorphism in lizard body shape: The roles of sexual selection and fecundity selection. Evolution 56, 1538–1542 (2002).Article 

    Google Scholar 
    4.McPherson, F. J. & Chenoweth, P. J. Mammalian sexual dimorphism. Anim. Reprod. Sci. 131, 109–122 (2012).Article 
    CAS 

    Google Scholar 
    5.Shine, R. The evolution of large body size in females: A critique of Darwin’s “fecundity advantage” model. Am. Nat. 131, 124–131 (1988).Article 

    Google Scholar 
    6.Fairbairn, D. J. et al. (eds) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism (Oxford University Press, 2007).
    Google Scholar 
    7.Slatkin, M. Ecological causes of sexual dimorphism. Evolution 38, 622–630 (1984).Article 

    Google Scholar 
    8.Shine, R. Ecological causes for the evolution of sexual dimorphism: A review of the evidence. Q. Rev. Biol. 64, 419–461 (1989).Article 
    CAS 

    Google Scholar 
    9.Herrel, A., Spithoven, L., Van Damme, R. & De Vree, F. Sexual dimorphism of head size in Gallotia galloti: Testing the niche divergence hypothesis by functional analyses. Funct. Ecol. 13, 289–297 (1999).Article 

    Google Scholar 
    10.Pearson, D., Shine, R. & How, R. Sex-specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata). Biol. J. Linn. Soc. 77, 113–125 (2002).Article 

    Google Scholar 
    11.Hierlihy, C. A., Garcia-Collazo, R., Chavez Tapia, C. B. & Mallory, F. F. Sexual dimorphism in the lizard Sceloporus siniferus: Support for the intraspecific niche divergence and sexual selection hypotheses. Salamandra 49, 1–6 (2013).
    Google Scholar 
    12.Vitt, L. J. & Cooper, W. E. Jr. The evolution of sexual dimorphism in the skink Eumeces laticeps: An example of sexual selection. Can. J. Zool. 63, 995–1002 (1985).Article 

    Google Scholar 
    13.Shine, R. Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am. Nat. 138, 103–122 (1991).Article 

    Google Scholar 
    14.Fitzgerald, M. & Shine, R. Mate-guarding in free-ranging Carpet Pythons (Morelia spilota). Aust. Zool. 39, 434–439 (2018).Article 

    Google Scholar 
    15.Cundall, D. & Greene, H. W. Feeding in snakes. In Feeding: Form, Function, and Evolution in Tetrapod Vertebrates (ed. Schwenk, K.) 293–333 (Academic Press, 2000).Chapter 

    Google Scholar 
    16.Goiran, C., Dubey, S. & Shine, R. Effects of season, sex and body size on the feeding ecology of turtle-headed sea snakes (Emydocephalus annulatus) on IndoPacific inshore coral reefs. Coral Reefs 32, 527–538 (2013).ADS 
    Article 

    Google Scholar 
    17.Shine, R., Bonnet, X., Elphick, M. J. & Barrott, E. G. A novel foraging mode in snakes: Browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Funct. Ecol. 18, 16–24 (2004).Article 

    Google Scholar 
    18.Lynch, T. P. The Behavioural Ecology of the Olive Sea Snake, Aipysurus laevis. PhD thesis, James Cook University (2000).19.Borczyk, B., Paśko, Ł, Kusznierz, J. & Bury, S. Sexual dimorphism and skull size and shape in the highly specialized snake species, Aipysurus eydouxii (Elapidae: Hydrophiinae). PeerJ 9, e11311 (2021).Article 

    Google Scholar 
    20.Queral-Regil, A. & King, R. B. Evidence for phenotypic plasticity in snake body size and relative head dimensions in response to amount and size of prey. Copeia 1998, 423–429 (1998).Article 

    Google Scholar 
    21.Bonnet, X., Shine, R., Naulleau, G. & Thiburce, C. Plastic vipers: influence of food intake on the size and shape of Gaboon vipers (Bitis gabonica). J. Zool. 255, 341–351 (2001).Article 

    Google Scholar 
    22.Sanders, K. L., Lee, M. S., Leys, R., Foster, R. & Keogh, J. S. Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): Evidence from seven genes for rapid evolutionary radiations. J. Evol. Biol. 21, 682–695 (2008).Article 
    CAS 

    Google Scholar 
    23.Aubret, F. & Shine, R. Genetic assimilation and the postcolonization erosion of phenotypic plasticity in island tiger snakes. Curr. Biol. 19, 1932–1936 (2009).Article 
    CAS 

    Google Scholar 
    24.McCarthy, C. J. Adaptations of sea snakes that eat fish eggs; with a note on the throat musculature of Aipysurus eydouxi (Gray, 1849). J. Nat. Hist. 21, 1119–1128 (1987).Article 

    Google Scholar 
    25.Shine, R., Shine, T. G., Brown, G. P. & Goiran, C. Life history traits of the sea snake Emydocephalus annulatus, based on a 17-yr study. Coral Reefs 39, 1407–1414 (2020).Article 

    Google Scholar 
    26.Segall, M., Cornette, R., Fabre, A. C., Godoy-Diana, R. & Herrel, A. Does aquatic foraging impact head shape evolution in snakes? Proc. R. Soc. B 283, 20161645 (2016).Article 

    Google Scholar 
    27.Avolio, C., Shine, R. & Pile, A. J. The adaptive significance of sexually dimorphic scale rugosity in sea snakes. Am. Nat. 167, 728–738 (2006).Article 

    Google Scholar 
    28.Sherratt, E., Rasmussen, A. R. & Sanders, K. L. Trophic specialization drives morphological evolution in sea snakes. R. Soc. Open Sci. 5, 172141 (2018).ADS 
    Article 

    Google Scholar 
    29.Frédérich, B. & Parmentier, E. (eds) Biology of Damselfishes (CRC Press, 2016).
    Google Scholar 
    30.Heatwole, H. Sea Snakes 2nd edn. (Krieger Publishing Company, 1999).
    Google Scholar 
    31.Lukoschek, V. & Shine, R. Sea snakes rarely venture far from home. Ecol. Evol. 2, 1113–1121 (2012).Article 

    Google Scholar 
    32.Shine, R., Shine, T. & Shine, B. Intraspecific habitat partitioning by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae): The effects of sex, body size, and colour pattern. Biol. J. Linn. Soc. 80, 1–10 (2003).Article 

    Google Scholar 
    33.Goiran, C., Brown, G. P. & Shine, R. Niche partitioning within a population of sea snakes is constrained by ambient thermal homogeneity and small prey size. Biol. J. Linn. Soc. 129, 644–651 (2020).Article 

    Google Scholar  More

  • in

    Seasonal variation in reversal learning reveals greater female cognitive flexibility in African striped mice

    Seasonal changes in weather, food availability and mice body conditionThe weather was hot and dry during summer (temperature: 24.42 ± 0.36 °C; total rainfall: 0.60 mm) and temperatures were lower and rainfall was higher during the winter months (temperature: 13.47 ± 0.45 °C; total rainfall: 39.60 mm; LM: N = 138, F = 368.4, P  More

  • in

    Urohidrosis as an overlooked cooling mechanism in long-legged birds

    1.Amat, J. A. & Masero, J. A. How Kentish plovers, Charadrius alexandrinus, cope with heat stress during incubation. Behav. Ecol. Sociobiol. 56, 26–33 (2004).Article 

    Google Scholar 
    2.du Plessis, K. L., Martin, R. O., Hockey, P. A. R., Cunningham, S. J. & Ridley, A. R. The costs of keeping cool in a warming world: Implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob. Chang. Biol. 18, 3063–3070 (2012).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Cunningham, S. J., Martin, R. O. & Hockey, P. A. R. Can behaviour buffer the impacts of climate change on an arid-zone bird?. Ostrich 86, 119–126 (2015).Article 

    Google Scholar 
    4.Smit, B. et al. Behavioural responses to heat in desert birds: implications for predicting vulnerability to climate warming. Clim. Chang. Responses 3, 1–14 (2016).Article 

    Google Scholar 
    5.McNab, B.K. The Physiological Ecology of Vertebrates: A View from Energetics (Cornell University Press, 2002).6.Cunningham, S. J., Gardner, J. L. & Martin, R. O. Opportunity costs and the response of birds and mammals to climate warming. Front. Ecol. Environ. 1, 1–8. https://doi.org/10.1002/fee.2324 (2021).Article 

    Google Scholar 
    7.Wolf, B. O., Wooden, K. M. & Walsberg, G. E. The use of thermal refugia by two small desert birds. Condor 98(2), 424–428 (1996).Article 

    Google Scholar 
    8.Cook, T. R. et al. Parenting in a warming world: Thermoregulatory responses to heat stress in an endangered seabird. Conserv. Physiol. 8, 1–13 (2020).Article 

    Google Scholar 
    9.Speakman, J. R. & Król, E. Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. J. Anim. Ecol. 79, 726–746 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    10.Nilsson, J. Å. & Nord, A. Testing the heat dissipation limit theory in a breeding passerine. Proc. R. Soc. B Biol. Sci. 285, 1 (2018).
    Google Scholar 
    11.Nord, A. & Nilsson, J. Å. Heat dissipation rate constrains reproductive investment in a wild bird. Funct. Ecol. 33, 250–259 (2019).Article 

    Google Scholar 
    12.Tapper, S., Nocera, J. J. & Burness, G. Heat dissipation capacity influences reproductive performance in an aerial insectivore. J. Exp. Biol. 223, 1 (2020).
    Google Scholar 
    13.Buckley, L. B., Ehrenberger, J. C. & Angilletta, M. J. Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change. Funct. Ecol. 29, 1038–1047 (2015).Article 

    Google Scholar 
    14.Edwards, E. K., Mitchell, N. J. & Ridley, A. R. The impact of high temperatures on foraging behaviour and body condition in the Western Australian Magpie Cracticus tibicen dorsalis. Ostrich 86, 137–144 (2015).Article 

    Google Scholar 
    15.Thompson, M. L., Cunningham, S. J. & McKechnie, A. E. Interspecific variation in avian thermoregulatory patterns and heat dissipation behaviours in a subtropical desert. Physiol. Behav. 188, 311–323 (2018).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    16.Kemp, R. et al. Sublethal fitness costs of chronic exposure to hot weather vary between sexes in a threatened desert lark. Emu 120, 216–229 (2020).Article 

    Google Scholar 
    17.Funghi, C., McCowan, L. S. C., Schuett, W. & Griffith, S. C. High air temperatures induce temporal, spatial and social changes in the foraging behaviour of wild zebra finches. Anim. Behav. 149, 33–43 (2019).Article 

    Google Scholar 
    18.Pattinson, N. B. et al. Heat dissipation behaviour of birds in seasonally hot arid-zones: are there global patterns?. J. Avian Biol. 51, 1–11 (2020).Article 

    Google Scholar 
    19.Moyer-Horner, L., Mathewson, P. D., Jones, G. M., Kearney, M. R. & Porter, W. P. Modeling behavioral thermoregulation in a climate change sentinel. Ecol. Evol. 5, 5810–5822 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Moore, D., Stow, A. & Kearney, M. R. Under the weather?—The direct effects of climate warming on a threatened desert lizard are mediated by their activity phase and burrow system. J. Anim. Ecol. 87, 660–671 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Bladon, A. J. et al. Behavioural thermoregulation and climatic range restriction in the globally threatened ethiopian bush-crow Zavattariornis stresemanni. Ibis 161(3), 546–558. https://doi.org/10.1111/ibi.12660 (2019).Article 

    Google Scholar 
    22.Conradie, S. R., Woodborne, S. M., Cunningham, S. J. & McKechnie, A. E. Chronic, sublethal effects of high temperatures will cause severe declines in southern African arid-zone birds during the 21st century. Proc. Natl. Acad. Sci. USA 116, 14065–14070 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    23.Enriquez-Urzelai, U. et al. The roles of acclimation and behaviour in buffering climate change impacts along elevational gradients. J. Anim. Ecol. 89, 1722–1734 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Albright, T. P. et al. Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc. Natl. Acad. Sci. USA 114, 2283–2288 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    25.Dawson, W. R. Evaporative losses of water by birds. Comp. Biochem. Physiol. Part A Physiol. 71, 495–509 (1982).Article 
    CAS 

    Google Scholar 
    26.Wolf, B. O. & Walsberg, G. E. Respiratory and cutaneous evaporative water loss at high environmental temperatures in a small bird. J. Exp. Biol. 199, 451–457 (1996).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    27.Calder, W. A. & Smichdt-Nielsen, K. Evaporative cooling and respiratory alkalosis in the pigeon. Proc. Natl. Acad. Sci. USA 55(4), 750–756. https://doi.org/10.1073/pnas.55.4.750 (1966).ADS 
    Article 
    PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    28.Bartholomew, G. A. The role of behavior in the temperature regulation of the masked booby. Condor 68, 523–535. https://doi.org/10.2307/1366261 (1966).Article 

    Google Scholar 
    29.Bryant, D. M. Heat stress in tropical birds: behavioural thermoregulation during flight. Ibis (Lond. 1859). 125, 313–323 (1983).30.Tattersall, G. J., Andrade, D. V. & Abe, A. S. Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science (80-. ). 325, 468–470 (2009).31.Van De Ven, T. M. F. N., Martin, R. O., Vink, T. J. F., McKechnie, A. E. & Cunningham, S. J. Regulation of heat exchange across the hornbill beak: Functional similarities with toucans?. PLoS ONE 11, 1–14 (2016).
    Google Scholar 
    32.Van Vuuren, A. K., Kemp, L. V. & McKechnie, A. E. The beak and unfeathered skin as heat radiators in the southern ground-hornbill. J. Avian Biol. 51, 1–7 (2020).
    Google Scholar 
    33.Winkler, D.W., Billerman, S.M. & Lovette, I.J. Storks (Ciconiidae), version 1.0. In Birds of the World (S. M. Billerman, B. K. Keeney, P. G. Rodewald, and T. S. Schulenberg, Editors). Cornell Lab of Ornithology (2020) https://doi.org/10.2173/bow.ciconi2.0134.Kahl, P. M. Thermoregulation in the wood stork, with special reference to the role of the legs. Physiol Zool. 36(2), 141–151 (1963).Article 

    Google Scholar 
    35.Steen, I. & Steen, J. B. The Importance of the Legs in the Thermoregulation of Birds. Acta Physiol. Scand. 63, 285–291 (1965).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    36.Hainsworth, F. R. Saliva spreading, activity and body temperature regulation in the rat. Am J Physiol. 212, 1288–1292 (1967).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    37.Gentry, R. L. Thermoregulatory behavior of eared seals. Behaviour 46(2), 73–93. https://doi.org/10.1163/156853973×00175 (1973).Article 
    PubMed 
    CAS 
    PubMed Central 

    Google Scholar 
    38.Sturbaum, B. A. & Riedesel, M. L. Dissipation of stored body heat by the ornate box turtle, Terrapene ornata. Comp. Biochem. Physiol. Part A Physiol. 58, 93–97 (1977).Article 

    Google Scholar 
    39.Marder, J., Porat, I., Raber, P. & Adler, J. Acid-base balance and body temperature regulation of heat stressed Psammomys obesus (Gerbillinae): The effect of bicarbonate loss via saliva spreading. Physiol Zool. 56(3), 389–396. https://doi.org/10.1086/physzool.56.3.30152603 (1983).Article 

    Google Scholar 
    40.Hatch, D. E. Energy conserving and heat dissipating mechanisms of the turkey vulture. Auk 87(1), 111–124. https://doi.org/10.2307/4083662 (1970).Article 

    Google Scholar 
    41.Cooper, J. & Siegfried, W. R. Behavioural responses of young cape gannets Sula capensis to high ambient temperatures. Mar. Behav. Physiol. 3, 211–220 (1976).Article 

    Google Scholar 
    42.Thomas, B. T. Maguari Stork Nesting: Juvenile Growth and Behavior. Auk 101, 812–823 (1984).Article 

    Google Scholar 
    43.Hancock, J.A., Kushlan, J.A. & Kahl, M.P. Storks, Ibises and Spoonbills of the World (Academic Press, 1992).44.Townsend, H., Huyvaert, K. P., Hodum, P. J. & Anderson, D. J. Nesting distributions of Galapagos boobies (Aves: Sulidae): an apparent case of amensalism. Oecologia 132, 419–427. https://doi.org/10.1007/s00442-002-0992-7 (2002).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Finkelstein, M., Kuspa, Z., Snyder, N.F. & Schmitt, N.J. California condor (Gymnogyps californianus), version 2.0. In The Birds of North America (P. G. Rodewald, Editor). Cornell Lab of Ornithology (2015). https://doi.org/10.2173/bna.61046.Czenze, Z. J. et al. Regularly drinking desert birds have greater evaporative cooling capacity and higher heat tolerance limits than non-drinking species. Funct. Ecol. 34, 1589–1600 (2020).Article 

    Google Scholar 
    47.Nudds, R. L. & Oswald, S. A. An interspecific test of Allen’s rule: Evolutionary implications for endothermic species. Evolution (N. Y). 61, 2839–2848 (2007).48.Symonds, M. R. E. & Tattersall, G. J. Geographical variation in bill size across bird species provides evidence for Allen’s rule. Am. Nat. 176, 188–197 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Galván, I., Rodríguez-Martínez, S. & Carrascal, L. M. Dark pigmentation limits thermal niche position in birds. Funct. Ecol. 32, 1531–1540 (2018).Article 

    Google Scholar 
    50.Wilman, H. et al. EltonTraits 1 . 0 : Species-level foraging attributes of the world ’ s birds and mammals. Ecology 95, 2027 (2014).51.Brooke, M. D. L. Ecological factors influencing the occurrence of ‘flash marks’ in wading birds. Funct. Ecol. 12, 339–346 (1998).Article 

    Google Scholar 
    52.Maclean, I. M. D., Mosedale, J. R. & Bennie, J. J. Microclima: An r package for modelling meso- and microclimate. Methods Ecol Evol. 10(2), 280–290. https://doi.org/10.1111/2041-210X.13093 (2019).Article 

    Google Scholar 
    53.Hadfield, A. J. Package ‘ MCMCglmm ’. https://cran.r-project.org/web/packages/MCMCglmm/ (2019)54.Jetz, W., Thomas, G.H., Joy, J.B., Hartmann, K. & Mooers, A.O. 2012. The global diversity of birds in space and time. Nature. 491(7424): 444–448 (2012). https://doi.org/10.1038/nature1163155.Revell, M.L.J. Package ‘ phytools ’ https://cran.r-project.org/web/packages/phytools/ (2020)56.Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: A test and review of evidence. Am. Nat. 160, 712–726 (2002).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    57.Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, (2015).58.Crawley, M.J. The R Book (John Wiley & Sons, 2013).59.Barton, K. Package MuMin: Multi-model Inference https://cran.r-project.org/web/packages/MuMIn/index.html (2020).60.Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: Challenges and solutions. J. Evol. Biol. 24, 699–711 (2011).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    61.Symonds, M. R. E. & Moussalli, A. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav. Ecol. Sociobiol. 65, 13–21 (2011).Article 

    Google Scholar 
    62.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/ (2020).63.Bakken, G. S. & Angilletta, M. J. How to avoid errors when quantifying thermal environments. Funct. Ecol. 28, 96–107 (2014).Article 

    Google Scholar 
    64.van Dyk, M., Noakes, M. J. & McKechnie, A. E. Interactions between humidity and evaporative heat dissipation in a passerine bird. J. Comp. Physiol. B. 189, 299–308. https://doi.org/10.1007/s00360-019-01210-2 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    65.Webster, M.D., Campbell, G.S. & King, J.R. Cutaneous resistance to water-vapor diffusion in pigeons and the role of the plumage. Physiol. Zool. 58(1): 58–70 (1985). http://www.jstor.org/stable/30161220.66.Battley, P. F., Rogers, D. I., Piersma, T. & Koolhaas, A. Behavioural evidence for heat-load problems in Great Knots in tropical Australia fuelling for long-distance flight. Emu 103, 97–103 (2003).Article 

    Google Scholar 
    67.Piersma, T. & van Gils, J.A. The Flexible Phenotype: A Body-Centered Integration of Ecology, Physiology, and Behavior (Oxford University Press, 2011).68.Fitzpatrick, M. J., Mathewson, P. D. & Porter, W. P. Validation of a mechanistic model for non-invasive study of ecological energetics in an endangered wading bird with counter-current heat exchange in its legs. PLoS ONE 10, 1–34 (2015).Article 
    CAS 

    Google Scholar 
    69.Lustick, S., Battersby, B. & Kelty, M. Effects of insolation on juvenile herring gull energetics and behavior. Ecologia. 60(4), 673–678. https://doi.org/10.2307/1936603 (1979).Article 

    Google Scholar 
    70.Ward, J. M., Blount, J. D., Ruxton, G. D. & Houston, D. C. The adaptive significance of dark plumage for birds in desert environments. Ardea 90, 311–323 (2002).
    Google Scholar 
    71.Nicolaï, M. P. J., Shawkey, M. D., Porchetta, S., Claus, R. & D’Alba, L. Exposure to UV radiance predicts repeated evolution of concealed black skin in birds. Nat. Commun. 11, (2020).72.Mitchell, D. et al. Revisiting concepts of thermal physiology: Predicting responses of mammals to climate change. J. Anim. Ecol. 87, 956–973 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Walsberg, G. E., Campbell, G. S. & King, J. R. Animal coat color and radiative heat gain: A re-evaluation. J. Comp. Physiol. B 126, 211–222 (1978).Article 

    Google Scholar 
    74.McFarland, D. J. & Baher, E. Factors affecting feather posture in the barbary dove. Anim. Behav. 16, 171–177 (1968).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    75.Hohtola, E., Rintamäki, H. & Hissa, R. Shivering and ptiloerection as complementary cold defense responses in the pigeon during sleep and wakefulness. J Comp Physiol. 136, 77–81. https://doi.org/10.1007/BF00688626 (1980).Article 

    Google Scholar 
    76.Kahl, P. M. Spread-wing postures and their possible functions in the Ciconiidae. Auk 88(4), 715–722. https://doi.org/10.2307/4083833 (1971).Article 

    Google Scholar 
    77.Dawson, T. J., Robertshaw, D. & Taylor, C. R. Sweating in the kangaroo: A cooling mechanism during exercise, but not in the heat. Am J Physiol. 227(2), 494–498. https://doi.org/10.1152/ajplegacy.1974.227.2.494 (1974).Article 
    PubMed 
    CAS 
    PubMed Central 

    Google Scholar 
    78.Hoffman, T. C. M., Walsberg, G. E. & DeNardo, D. F. Cloacal evaporation: an important and previously undescribed mechanism for avian thermoregulation. J. Exp. Biol. 210, 741–749 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    79.Graves, G. R. Urohidrosis and tarsal color in Cathartes vultures (Aves: Cathartidae). Proc. Biol. Soc. Washingt. 132, 56–64 (2019).Article 

    Google Scholar 
    80.Torres, R. & Velando, A. Male preference for female foot colour in the socially monogamous blue-footed booby, Sula nebouxii.. Anim. Behav. 69, 59–65 (2005).Article 

    Google Scholar 
    81.López-Rull, I., Lifshitz, N., Macías Garcia, C., Graves, J. A. & Torres, R. Females of a polymorphic seabird dislike foreign-looking males. Anim. Behav. 113, 31–38 (2016).82.Gutiérrez, J. S. & Soriano-Redondo, A. Laterality in foraging phalaropes promotes phenotypically assorted groups. Behav. Ecol. 31, 1429–1435 (2021).Article 

    Google Scholar 
    83.Jarić, I. et al. iEcology: Harnessing large online resources to generate ecological insights. Trends Ecol. Evol. 35, 630–639 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Vrettos, M., Reynolds, C. & Amar, A. Malar stripe size and prominence in peregrine falcons vary positively with solar radiation: support for the solar glare hypothesis. Biol. Lett. 17, 20210116. https://doi.org/10.1098/rsbl.2021.0116 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    SNP markers reveal relationships between fruit paternity, fruit quality and distance from a cross-pollen source in avocado orchards

    1.Ashman, T.-L. et al. Pollen limitation of plant reproduction: Ecological and evolutionary causes and consequences. Ecology 85, 2408–2421 (2004).Article 

    Google Scholar 
    2.Ricketts, T. H. et al. Landscape effects on crop pollination services: Are there general patterns?. Ecol. Lett. 11, 499–515 (2008).Article 

    Google Scholar 
    3.Rollin, O. & Garibaldi, L. A. Impacts of honeybee density on crop yield: A meta-analysis. J. Appl. Ecol. 56, 1152–1163. https://doi.org/10.1111/1365-2664.13355 (2019).Article 

    Google Scholar 
    4.Bennett, J. M. et al. Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene. Nat. Commun. 11, 3999. https://doi.org/10.1038/s41467-020-17751-y (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Aizen, M. A. & Harder, L. D. Expanding the limits of the pollen-limitation concept: Effects of pollen quantity and quality. Ecology 88, 271–281 (2007).Article 

    Google Scholar 
    6.Igic, B. & Kohn, J. R. The distribution of plant mating systems: Study bias against obligately outcrossing species. Evolution 60, 1098–1103 (2006).Article 

    Google Scholar 
    7.Abrol, D. P. Pollination Biology: Biodiversity and Conservation and Agricultural Production. Applied Pollination: Present Scenario 55–83 (Springer, 2012).
    Google Scholar 
    8.Frankel, R. & Galun, E. Pollination Mechanisms, Reproduction and Plant Breeding Vol. 2 (Springer Verlag, 1977).Book 

    Google Scholar 
    9.Schneider, D., Goldway, M., Rotman, N., Adato, I. & Stern, R. A. Cross-pollination improves ‘Orri’ mandarin fruit yield. Sci. Hortic. 122, 380–384 (2009).Article 

    Google Scholar 
    10.Fattahi, R., Mohammadzedeh, M. & Khadivi-Khub, A. Influence of different pollen sources on nut and kernel characteristics of hazelnut. Sci. Hortic. 173, 15–19 (2014).Article 

    Google Scholar 
    11.Żurawicz, E., Studnicki, M., Kubik, J. & Pruski, K. A careful choice of compatible pollinizers significantly improves the size of fruits in red raspberry (Rubus idaeus L.). Sci. Hortic. 235, 253–257 (2018).Article 

    Google Scholar 
    12.Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611. https://doi.org/10.1126/science.1230200 (2013).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Willcox, B. K., Aizen, M. A., Cunningham, S. A., Mayfield, M. M. & Rader, R. Deconstructing pollinator community effectiveness. Curr. Opin. Insect. Sci. 21, 98–104. https://doi.org/10.1016/j.cois.2017.05.012 (2017).Article 
    PubMed 

    Google Scholar 
    14.Richards, T. E. et al. Relationships between nut size, kernel quality, nutritional composition and levels of outcrossing in three macadamia cultivars. Plants 9, 228 (2020).CAS 
    Article 

    Google Scholar 
    15.van Nocker, S. & Gardiner, S. E. Breeding better cultivars, faster: Applications of new technologies for the rapid deployment of superior horticultural tree crops. Hortic. Res. 1, 14022. https://doi.org/10.1038/hortres.2014.22 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Isaacs, R. & Kirk, A. K. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J. Appl. Ecol. 47, 841–849 (2010).Article 

    Google Scholar 
    17.Brittain, C., Kremen, C., Garber, A. & Klein, A.-M. Pollination and plant resources change the nutritional quality of almonds for human health. PLoS ONE 9, e90082. https://doi.org/10.1371/journal.pone.0090082 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.Klatt, B. K. et al. Bee pollination improves crop quality, shelf life and commercial value. Proc. R. Soc. B 281, 20132440 (2014).Article 

    Google Scholar 
    19.Crane, J. et al. in The Avocado: Botany, Production and Uses (eds. Schaffer, B., Wolstenholme, B. N. & Whiley, A. W.) 200–233 (CABI, 2013).20.Duarte, P. F., Chaves, M. A., Borges, C. D. & Mendonça, C. R. B. Avocado: Characteristics, health benefits and uses. Ciênc. Rural 46, 747–754. https://doi.org/10.1590/0103-8478cr20141516 (2016).CAS 
    Article 

    Google Scholar 
    21.Dreher, M. L. & Davenport, A. J. Hass avocado composition and potential health effects. Crit. Rev. Food Sci. Nutr. 53, 738–750. https://doi.org/10.1080/10408398.2011.556759 (2013).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Araújo, R. G., Rodriguez-Jasso, R. M., Ruiz, H. A., Pintado, M. M. E. & Aguilar, C. N. Avocado by-products: Nutritional and functional properties. Trends Food Sci. Technol. 80, 51–60. https://doi.org/10.1016/j.tifs.2018.07.027 (2018).CAS 
    Article 

    Google Scholar 
    23.Lerman-Garber, I., Ichazo-Cerro, S., Zamora-González, J., Cardoso-Saldaña, G. & Posadas-Romero, C. Effect of a high-monounsaturated fat diet enriched with avocado in NIDDM patients. Diabetes Care 17, 311–315. https://doi.org/10.2337/diacare.17.4.311 (1994).CAS 
    Article 
    PubMed 

    Google Scholar 
    24.López, L. R. et al. Monounsaturated fatty acid (avocado) rich diet for mild hypercholesterolemia. Arch. Med. Res. 27, 519–523 (1996).
    Google Scholar 
    25.Kris-Etherton, P. M. et al. High-monounsaturated fatty acid diets lower both plasma cholesterol and triacylglycerol concentrations. Am. J. Clin. Nutr. 70, 1009–1015 (1999).CAS 
    Article 

    Google Scholar 
    26.Trueman, S. J., Richards, S., McConchie, C. A. & Turnbull, C. G. N. Relationships between kernel oil content, fruit removal force and abscission in macadamia. Aust. J. Exp. Agric. 40, 859–866 (2000).Article 

    Google Scholar 
    27.Stout, A. B. A Study in Cross-Pollination of Avocados in Southern California (New York Botanical Garden, 1923).
    Google Scholar 
    28.Blanke, M. M. & Lovatt, C. J. Anatomy and transpiration of the avocado inflorescence. Ann. Bot. 71, 543–547. https://doi.org/10.1006/anbo.1993.1070 (1993).Article 

    Google Scholar 
    29.Salazar-García, S., Garner, L. C. & Lovatt, C. J. in The Avocado: Botany, Production and Uses. Reproductive Biology (eds. Schaffer, B., Wolstenholme, B. N. & Whiley, A. W.) 118–167 (CABI, 2013).30.Garner, L. C. & Lovatt, C. J. The relationship between flower and fruit abscission and alternate bearing of ‘Hass’ avocado. J. Am. Soc. Hortic. Sci. 133, 3–10. https://doi.org/10.21273/jashs.133.1.3 (2008).Article 

    Google Scholar 
    31.Vithanage, V. The role of the European honeybee (Apis mellifera L.) in avocado pollination. J. Hortic. Sci. 65, 81–86. https://doi.org/10.1080/00221589.1990.11516033 (1990).Article 

    Google Scholar 
    32.Perez-Balam, J. et al. The contribution of honey bees, flies and wasps to avocado (Persea americana) pollination in southern Mexico. J. Pollinat. Ecol. 8, 42–47 (2012).Article 

    Google Scholar 
    33.Ying, Z., Davenport, T. L. R., Zhang, T., Schnell, R. J. & Tondo, C. L. Selection of highly informative microsatellite markers to identify pollen donors in “Hass” avocado orchards. Plant Mol. Biol. Rep. 27, 374–380 (2009).CAS 
    Article 

    Google Scholar 
    34.Alcaraz, M. & Hormaza, J. Influence of physical distance between cultivars on yield, outcrossing rate and selective fruit drop in avocado (Persea americana, Lauraceae). Ann. Appl. Biol. 158, 354–361 (2011).Article 

    Google Scholar 
    35.Borrone, J. W. et al. Outcrossing in Florida avocados as measured using microsatellite markers. J. Am. Soc. Hortic. Sci. 133, 255–261 (2008).Article 

    Google Scholar 
    36.Schnell, R. J. et al. Outcrossing between ‘Bacon’ pollinizers and adjacent ‘Hass’ avocado trees and the description of two new lethal mutants. HortScience 44, 1522. https://doi.org/10.21273/hortsci.44.6.1522 (2009).Article 

    Google Scholar 
    37.Degani, C., Goldring, A., Adato, I., El-Batsri, R. & Gazit, S. Pollen parent effect on outcrossing rate, yield, and fruit characteristics of `Fuerte’ avocado. HortScience 25, 471. https://doi.org/10.21273/hortsci.25.4.471 (1990).Article 

    Google Scholar 
    38.Sedgley, M. & Annells, C. M. Flowering and fruit-set response to temperature in the avocado cultivar ‘Hass’. Sci. Hortic. 14, 27–33. https://doi.org/10.1016/0304-4238(81)90075-3 (1981).Article 

    Google Scholar 
    39.Degani, C., El-Batsri, R. & Gazit, S. Outcrossing rate, yield, and selective fruit abscission in “Ettinger” and “Ardith” avocado plots. J. Am. Soc. Hortic. Sci. 122, 813–817 (1997).Article 

    Google Scholar 
    40.Ying, Z. et al. Re-evaluation of the roles of honeybees and wind on pollination in avocado. J. Hortic. Sci. Biotechnol. 84, 255–260. https://doi.org/10.1080/14620316.2009.11512513 (2009).Article 

    Google Scholar 
    41.Sapir, G. et al. Synergistic effects between bumblebees and honey bees in apple orchards increase cross pollination, seed number and fruit size. Sci. Hortic. 219, 107–117. https://doi.org/10.1016/j.scienta.2017.03.010 (2017).Article 

    Google Scholar 
    42.Stern, R., Eisikowitch, D. & Dag, A. Sequential introduction of honeybee colonies and doubling their density increases cross-pollination, fruit-set and yield in ‘Red Delicious’ apple. J. Hortic. Sci. Biotechnol. 76, 17–23. https://doi.org/10.1080/14620316.2001.11511320 (2001).Article 

    Google Scholar 
    43.Kämper, W., Trueman, S. J., Ogbourne, S. M. & Wallace, H. M. Pollination services in macadamia depend on across-orchard transport of cross pollen. J. Appl. Ecol. (under review).44.Robbertse, P. J., Coetzer, L. A., Johannsmeier, M. F., Köhne, J. S. & Morudu, T. M. Hass Yield and Fruit Size as Influenced by Pollination and Pollen Donor—A Joint Progress Report 63–67 (South African Avocado Growers’ Association Yearbook, 1996).
    Google Scholar 
    45.Araújo, E., Costa, M., Chaud-Netto, J. & Fowler, H. G. Body size and flight distance in stingless bees (Hymenoptera: Meliponini): Inference of flight range and possible ecological implications. Braz. J. Biol. 64, 563–568 (2004).Article 

    Google Scholar 
    46.Jalali-Khanabadi, B.-A., Mozaffari-Khosravi, H. & Parsaeyan, N. Effects of almond dietary supplementation on coronary heart disease lipid risk factors and serum lipid oxidation parameters in men with mild hyperlipidemia. J. Altern. Complement. Med. 16, 1279–1283 (2010).Article 

    Google Scholar 
    47.Kaiser, C. & Wolstenholme, B. N. Aspects of delayed harvest of ‘Hass’ avocado (Persea americana Mill.) fruit in a cool subtropical climate. I. Fruit lipid and fatty acid accumulation. J. Hortic. Sci. 69, 437–445. https://doi.org/10.1080/14620316.1994.11516473 (1994).CAS 
    Article 

    Google Scholar 
    48.Smil, V. Phosphorus in the environment: Natural flows and human interferences. Annu. Rev. Environ. Resour. 25, 53–88. https://doi.org/10.1146/annurev.energy.25.1.53 (2000).Article 

    Google Scholar 
    49.Bangerth, F. Calcium-related physiological disorders of plants. Annu. Rev. Phytopathol. 17, 97–122. https://doi.org/10.1146/annurev.py.17.090179.000525 (1979).CAS 
    Article 

    Google Scholar 
    50.Witney, G. W., Hofman, P. J. & Wolstenholme, B. N. Effect of cultivar, tree vigour and fruit position on calcium accumulation in avocado fruits. Sci. Hortic. 44, 269–278. https://doi.org/10.1016/0304-4238(90)90127-Z (1990).CAS 
    Article 

    Google Scholar 
    51.Matoh, T. & Kobayashi, M. Boron and calcium, essential inorganic constituents of pectic polysaccharides in higher plant cell walls. J. Plant Res. 111, 179–190 (1998).CAS 
    Article 

    Google Scholar 
    52.Hopkirk, G., White, A., Beever, D. J. & Forbes, S. K. Influence of postharvest temperatures and the rate of fruit ripening on internal postharvest rots and disorders of New Zealand ‘Hass’ avocado fruit. N. Z. J. Crop Hortic. Sci. 22, 305–311. https://doi.org/10.1080/01140671.1994.9513839 (1994).Article 

    Google Scholar 
    53.Meir, S. et al. Prolonged storage of `Hass’ avocado fruit using modified atmosphere packaging. Postharvest Biol. Technol. 12, 51–60. https://doi.org/10.1016/S0925-5214(97)00038-0 (1997).CAS 
    Article 

    Google Scholar 
    54.Flitsanov, U., Mizrach, A., Liberzon, A., Akerman, M. & Zauberman, G. Measurement of avocado softening at various temperatures using ultrasound. Postharvest Biol. Technol. 20, 279–286 (2000).Article 

    Google Scholar 
    55.Hofman, P. J., Bower, J. & Woolf, A. in The Avocado: Botany, Production and Uses. Harvesting, Packing, Postharvest Technology, Transport and Processing (eds. Schaffer, B., Wolstenholme, B. N. & Whiley, A. W.) 489–540 (CABI, 2013).56.McGeehan, S. L. & Naylor, D. V. Automated instrumental analysis of carbon and nitrogen in plant and soil samples. Commun. Soil Sci. Plant Anal. 19, 493–505. https://doi.org/10.1080/00103628809367953 (1988).CAS 
    Article 

    Google Scholar 
    57.Rayment, G. E. & Higginson, F. R. Australian Laboratory Handbook of Soil and Water Chemical Methods (Inkata, 1992).
    Google Scholar 
    58.Munter, R. C. & Grande, R. A. in Developments in Atomic Plasma Spectrochemical Analysis. Plant Tissue and Soil Extract Analysis by ICP-Atomic Emission Spectrometry (ed. Byrnes, R. M.) 653–672 (Heyden, 1981).59.Martinie, G. D. & Schilt, A. A. Wet oxidation efficiencies of perchloric acid mixtures for various organic substances and the identities of residual matter. Anal. Chem. 48, 70–74. https://doi.org/10.1021/ac60365a032 (1976).CAS 
    Article 

    Google Scholar 
    60.Bai, S. H. et al. Nutritional quality of almond, canarium, cashew and pistachio and their oil photooxidative stability. J. Food Sci. Technol. 56, 792–798. https://doi.org/10.1007/s13197-018-3539-6 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    61.Ivanova, N. V., Fazekas, A. J. & Hebert, P. D. N. Semi-automated, membrane-based protocol for DNA isolation from plants. Plant Mol. Biol. Rep. 26, 186–198 (2008).CAS 
    Article 

    Google Scholar 
    62.Kämper, W., Cooke, J., Trueman, S. J. & Ogbourne, S. M. Detection of single nucleotide polymorphisms (SNPs) in avocado cultivars, Persea americana (Lauraceae). Appl. Plant Sci. (submitted).63.Jordon-Thaden, I. E. et al. A basic ddRADseq two-enzyme protocol performs well with herbarium and silica-dried tissues across four genera. Appl. Plant Sci. 8, e11344–e11344. https://doi.org/10.1002/aps3.11344 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Sharon, D. et al. An integrated genetic linkage map of avocado. Theor. Appl. Genet. 95, 911–921 (1997).CAS 
    Article 

    Google Scholar 
    65.Borrone, J. W., Schnell, R. J., Violi, H. A. & Ploetz, R. C. Seventy microsatellite markers from Persea americana Miller (avocado) expressed sequence tags. Mol. Ecol. Resour. 7, 439–444 (2007).CAS 
    Article 

    Google Scholar 
    66.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).
    Google Scholar 
    67.Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar  More

  • in

    Isotope data from amino acids indicate Darwin’s ground sloth was not an herbivore

    1.Voss, R. S. & Emmons, L. H. Mammalian diversity in Neotropical lowland rainforests: A preliminary assessment. Bull. Am. Museum Nat. Hist. 230, 1–115 (1996).
    Google Scholar 
    2.Barnosky, A. D. et al. Variable impact of late-Quaternary megafaunal extinction in causing ecological state shifts in North and South America. Proc. Natl. Acad. Sci. U. S. A. 113, 856–861 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Croft, D. A., Engelman, R. K., Dolgushina, T. & Wesley, G. Diversity and disparity of sparassodonts (Metatheria) reveal non-analogue nature of ancient South American mammalian carnivore guilds. Proc. R. Soc. B 285, 20172012 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Fariña, R. A. Trophic relationships among Lujanian mammals. Evol. Theory 11, 125–134 (1996).
    Google Scholar 
    5.Fariña, R. A. & Blanco, R. E. Megatherium the Stabber. Proc. R. Soc. B Biol. Sci. 263, 1725–1729 (2006).ADS 

    Google Scholar 
    6.Tejada-Lara, J. V. et al. Body mass predicts isotope enrichment in herbivorous mammals. Proc. R. Soc. B Biol. Sci. 285, 20181020 (2018).Article 
    CAS 

    Google Scholar 
    7.de Muizon, C. & McDonald, H. G. An aquatic sloth from the Pliocene of Peru. Nature 375, 224–227 (1995).ADS 
    Article 

    Google Scholar 
    8.Croft, D. A. The middle Miocene (Laventan) Quebrada Honda Fauna, southern Bolivia and a description of its notoungulates. Palaeontology 50, 277–303 (2007).Article 

    Google Scholar 
    9.Boecklen, W. J., Yarnes, C. T., Cook, B. A. & James, A. C. On the use of stable isotopes in trophic ecology. Annu. Rev. Ecol. Evol. Syst. 42, 411–440 (2011).Article 

    Google Scholar 
    10.Lee-Thorp, J. J., Sealy, J. J. C. & van der Merwe, N. J. N. Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J. Archaeol. Sci. 32, 1459–1470 (1989).
    Google Scholar 
    11.Clementz, M. T., Fox-Dobbs, K., Wheatley, P. V., Koch, P. L. & Doak, D. F. Revisiting old bones: Coupled carbon isotope analysis of bioapatite and collagen as an ecological and palaeoecological tool. Geol. J. 44, 605–620 (2009).CAS 
    Article 

    Google Scholar 
    12.Tejada, J. V. et al. Comparative isotope ecology of western Amazonian rainforest mammals. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.2007440117 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Robinson, D. δ15N as an integrator of the nitrogen cycle. Trends Ecol. Evol. 16, 153–162 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    14.McMahon, K. W. & McCarthy, M. D. Embracing variability in amino acid δ15N fractionation: Mechanisms, implications, and applications for trophic ecology. Ecosphere 7, 1–26 (2016).Article 

    Google Scholar 
    15.McClelland, J. W. & Montoya, J. P. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173–2180 (2002).Article 

    Google Scholar 
    16.Chikaraishi, Y., Ogawa, N. O., Doi, H. & Ohkouchi, N. 15N/14N ratios of amino acids as a tool for studying terrestrial food webs: A case study of terrestrial insects (bees, wasps, and hornets ). Ecol. Res. 26, 835–844 (2011).Article 

    Google Scholar 
    17.Popp, B. N. et al. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound- specific nitrogen isotope analysis of proteinaceous amino acids. In Stable Isotopes as Indicators of Ecological Change (eds Dawson, T. E. & Siegwolf, R. T. W.) 173–190 (Elsevier Inc., 2007).
    Google Scholar 
    18.Naito, Y. I., Honch, N. V., Chikaraishi, Y., Ohkouchi, N. & Yoneda, M. Quantitative evaluation of marine protein contribution in ancient diets based on nitrogen isotope ratios of individual amino acids in bone collagen: An investigation at the Kitakogane Jomon Site. Am. J. Phys. Anthropol. 143, 31–40 (2010).PubMed 
    Article 

    Google Scholar 
    19.O’Connell, T. C. ‘Trophic’ and ‘source’ amino acids in trophic estimation: A likely metabolic explanation. Oecologia 184, 317–326 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Chikaraishi, Y., Ogawa, N. O. & Ohkouchi, N. Further evaluation of the trophic level estimation based on nitrogen isotopic composition of amino acids. In Earth, Life, and Isotopes (eds Ohkouchi, N. et al.) 37–51 (Kyoto Universy Press, 2010).
    Google Scholar 
    21.Steffan, S. A. et al. Trophic hierarchies illuminated via amino acid isotopic analysis. PLoS ONE 8, 1–10 (2013).Article 
    CAS 

    Google Scholar 
    22.Chikaraishi, Y., Kashiyama, Y., Ogawa, N. O., Kitazato, H. & Ohkouchi, N. Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: Implications for aquatic food web studies. Mar. Ecol. Prog. Ser. 342, 85–90 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    23.Naito, Y. I. et al. Ecological niche of Neanderthals from Spy Cave revealed by nitrogen isotopes of individual amino acids in collagen. J. Hum. Evol. 93, 82–90 (2016).PubMed 
    Article 

    Google Scholar 
    24.Nielsen, J. M., Popp, B. N. & Winder, M. Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia https://doi.org/10.1007/s00442-015-3305-7 (2015).Article 
    PubMed 

    Google Scholar 
    25.Décima, M., Landry, M. R. & Popp, B. N. Environmental perturbation effects on baseline δ15N values and zooplankton trophic flexibility in the southern California current ecosystem. Limnol. Oceanogr. 58, 624–634 (2013).ADS 
    Article 
    CAS 

    Google Scholar 
    26.Jarman, C. L. et al. Diet of the prehistoric population of Rapa Nui (Easter Island, Chile) shows environmental adaptation and resilience. Am. J. Phys. Anthropol. https://doi.org/10.1002/ajpa.23273 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Kendall, I. P. et al. Compound-specific δ15N values express differences in amino acid metabolism in plants of varying lignin content. Phytochemistry 161, 130–138 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Ramirez, M. D., Besser, A. C., Newsome, S. D. & McMahon, K. W. Meta-analysis of primary producer amino acid δ15N values and their influence on trophic position estimation. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13678 (2021).Article 

    Google Scholar 
    29.Hebert, C. E., Popp, B. N., Fernie, K. J., Rattner, B. A. & Wallsgrove, N. Amino acid specific stable nitrogen isotope values in avian tissues: Insights from captive American kestrels and wild herring gulls. Environ. Sci. Technol. 50, 12928–12937 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Chikaraishi, Y. et al. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr. 7, 740–750 (2009).CAS 
    Article 

    Google Scholar 
    31.Steffan, S. A. et al. Microbes are trophic analogs of animals. Proc. Natl. Acad. Sci. 112, 15119–15124 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Kendall, I. P., Lee, M. R. F. & Evershed, R. P. The effect of trophic level on individual amino acid δ15N values in a terrestrial ruminant food web. Sci. Technol. Archaeol. Res. 3, 135–145 (2017).
    Google Scholar 
    33.Matthews, C. J. D., Ruiz-Cooley, R. I., Pomerleau, C. & Ferguson, S. H. Amino acid δ15N underestimation of cetacean trophic positions highlights limited understanding of isotopic fractionation in higher marine consumers. Ecol. Evol. 10, 3450–3462 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Styring, A. K., Sealy, J. C. & Evershed, R. P. Resolving the bulk δ15N values of ancient human and animal bone collagen via compound-specific nitrogen isotope analysis of constituent amino acids. Geochim. Cosmochim. Acta 74, 241–251 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    35.Lorrain, A. et al. Nitrogen and carbon isotope values of individual amino acids: A tool to study foraging ecology of penguins in the Southern Ocean. Mar. Ecol. Prog. Ser. 391, 293–306 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Lorrain, A. et al. Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep. Res. Part II Top. Stud. Oceanogr. 113, 188–198 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    37.Hartman, G. Are elevated δ15N values in herbivores in hot and arid environments caused by diet or animal physiology?. Funct. Ecol. 25, 122–131 (2011).Article 

    Google Scholar 
    38.Hartman, G. & Danin, A. Isotopic values of plants in relation to water availability in the Eastern Mediterranean region. Oecologia 162, 837–852 (2010).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Hansen, R. M. Shasta ground sloth food habits, Rampart Cave, Arizona. Paleobiology 4, 302–319 (1978).Article 

    Google Scholar 
    40.McDonald, H. G. & Morgan, G. S. Ground Sloths of New Mexico. Foss. Rec. 3 New. Mex. Museum Nat. Hist. Sci. Bull. 53, 652–663 (2011).
    Google Scholar 
    41.Poinar, H. N. Molecular coproscopy: Dung and diet of the extinct ground sloth Nothrotheriops shastensis. Science 281, 402–406 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Clack, A. A., MacPhee, R. D. E. & Poinar, H. N. Mylodon darwinii DNA sequences from ancient fecal hair shafts. Ann. Anat. 194, 26–30 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Höss, M., Dilling, A., Currant, A. & Pääbo, S. Molecular phylogeny of the extinct ground sloth Mylodon darwinii. Proc. Natl. Acad. Sci. U. S. A. 93, 181–185 (1996).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Moore, D. M. Post-glacial vegetation in the South Patagonian territory of the giant ground sloth, Mylodon. Bot. J. Linn. Soc. 77, 177–202 (1978).Article 

    Google Scholar 
    45.Bargo, M. S., Toledo, N. & Vizcaino, S. F. Muzzle of South American Pleistocene ground sloths (Xenarthra, Tardigrada). J. Morphol. 267, 248–263 (2006).PubMed 
    Article 

    Google Scholar 
    46.Rasmussen, M. et al. Response to comment by Goldberg et al. on ‘DNA from Pre-Clovis human coprolites in Oregon, North America’. Science 325, 148 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    47.Janis, C. M. Correlations between craniodental anatomy and feeding in ungulates: Reciprocal illumination between living and fossil taxa. In Functional Morphology in Vertebrate Paleontology (ed. Thomason, J.) 76–98 (Cambridge U Press, 1995).
    Google Scholar 
    48.Clauss, M., Nunn, C., Fritz, J. & Hummel, J. Evidence for a tradeoff between retention time and chewing efficiency in large mammalian herbivores. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 154, 376–382 (2009).PubMed 
    Article 
    CAS 

    Google Scholar 
    49.Vizcaino, S. F., Bargo, M. S. & Cassini, G. H. Dental occlusal surface area in relation to body mass, food habits and other biologic features in fossil xenarthrans. Ameghiniana 43, 11–26 (2006).
    Google Scholar 
    50.McNab, B. K. Energetics, population biology, and distribution of xenarthrans, living and extinct. In The Ecology of Arboreal Folivores 219–232 (Smithsonian Press, 1985).51.Davis, L. B. & Birkbak, R. C. On the transfer of energy in layers of fur. Biophys. J. 14, 249–268 (1974).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Clauss, M. et al. The maximum attainable body size of herbivorous mammals: Morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136, 14–27 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Fariña, R. A., Czerwonogora, A. & Di Giacomo, M. Splendid oddness: Revisiting the curious trophic relationships of South American Pleistocene mammals and their abundance. An. Acad. Bras. Cienc. 86, 311–331 (2014).PubMed 
    Article 

    Google Scholar 
    54.Zhu, D. et al. The large mean body size of mammalian herbivores explains the productivity paradox during the Last Glacial Maximum. Nat. Ecol. Evol. 2, 640–649 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Zimov, S. A., Zimov, N. S., Tikhonov, A. N. & Chapin, I. S. Mammoth steppe: A high-productivity phenomenon. Quat. Sci. Rev. 57, 26–45 (2012).ADS 
    Article 

    Google Scholar 
    56.Hannides, C. C. S., Popp, B. N., Landry, M. R. & Graham, B. S. Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol. Oceanogr. 54, 50–61 (2009).ADS 
    CAS 
    Article 

    Google Scholar  More

  • in

    Coral micro- and macro-morphological skeletal properties in response to life-long acclimatization at CO2 vents in Papua New Guinea

    1.Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science (80-.) 318, 1737–1742 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    2.Roberts, M., Hanley, N., Williams, S. & Cresswell, W. Terrestrial degradation impacts on coral reef health: Evidence from the Caribbean. Ocean Coast. Manag. 149, 52–68 (2017).Article 

    Google Scholar 
    3.Mollica, N. R. et al. Ocean acidification affects coral growth by reducing skeletal density. Proc. Natl. Acad. Sci. 115, 1754–1759 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Ries, J. B. Skeletal mineralogy in a high-CO2 world. J. Exp. Mar. Biol. Ecol. 403, 54–64 (2011).CAS 
    Article 

    Google Scholar 
    5.Erez, J., Reynaud, S., Silverman, J., Schneider, K. & Allemand, D. Coral calcification under ocean acidification and global change. In Coral Reefs: An Ecosystem in Transition (2011). https://doi.org/10.1007/978-94-007-0114-4_10.6.Dove, S. G. et al. Future reef decalcification under a business-as-usual CO2 emission scenario. Proc. Natl. Acad. Sci. 110, 15342–15347 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Cooper, T. F., De’ath, G., Fabricius, K. E. & Lough, J. M. Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Glob. Chang. Biol. 14, 529–538 (2008).ADS 
    Article 

    Google Scholar 
    8.Cooper, T. F., O’Leary, R. A. & Lough, J. M. Growth of Western Australian corals in the Anthropocene. Science (80-.) 335, 593–596 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Teixidó, N. et al. Ocean acidification causes variable trait-shifts in a coral species. Glob. Chang. Biol. https://doi.org/10.1111/gcb.15372 (2020).Article 
    PubMed 

    Google Scholar 
    10.Pandolfi, J. M. Incorporating uncertainty in predicting the future response of coral reefs to climate change. Annu. Rev. Ecol. Evol. Syst. 46, 281–303 (2015).Article 

    Google Scholar 
    11.Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).PubMed 
    Article 

    Google Scholar 
    12.Jokiel, P. L. et al. Ocean acidification and calcifying reef organisms: A mesocosm investigation. Coral Reefs 27, 473–483 (2008).ADS 
    Article 

    Google Scholar 
    13.Fantazzini, P. et al. Gains and losses of coral skeletal porosity changes with ocean acidification acclimation. Nat. Commun. 6, 7785 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Wittmann, A. C. & Pörtner, H.-O. Sensitivities of extant animal taxa to ocean acidification. Nat. Clim. Chang. 3, 995–1001 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    15.Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Chang. 1, 165–169 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    16.Riebesell, U. Acid test for marine biodiversity. Nature 454, 46–47 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    17.Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96–99 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Johnson, V. R., Russell, B. D., Fabricius, K. E., Brownlee, C. & Hall-Spencer, J. M. Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob. Chang. Biol. https://doi.org/10.1111/j.1365-2486.2012.02716.x (2012).Article 
    PubMed 

    Google Scholar 
    19.Prada, F. et al. Ocean warming and acidification synergistically increase coral mortality. Sci. Rep. 7, 1–10 (2017).ADS 
    MathSciNet 
    Article 
    CAS 

    Google Scholar 
    20.Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Chang. 3, 683–687 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    21.Crook, E. D., Cohen, A. L., Rebolledo-Vieyra, M., Hernandez, L. & Paytan, A. Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification. Proc. Natl. Acad. Sci. 110, 11044–11049 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Teixidó, N. et al. Functional biodiversity loss along natural CO2 gradients. Nat. Commun. 9, 5149 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    23.Strahl, J. et al. Physiological and ecological performance differs in four coral taxa at a volcanic carbon dioxide seep. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 184, 179–186 (2015).CAS 
    Article 

    Google Scholar 
    24.Fabricius, K. E., De’ath, G., Noonan, S. & Uthicke, S. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. B Biol. Sci. 281, 20132479 (2014).CAS 
    Article 

    Google Scholar 
    25.Fabricius, K. E., Noonan, S. H. C., Abrego, D., Harrington, L. & De’ath, G. Low recruitment due to altered settlement substrata as primary constraint for coral communities under ocean acidification. Proc. R. Soc. B Biol. Sci. 284, 20171536 (2017).Article 
    CAS 

    Google Scholar 
    26.Siahainenia, L., Tuhumury, S. F., Uneputty, P. A. & Tuhumury, N. C. Survival and growth of transplanted coral reef in lagoon ecosystem of Ihamahu, Central Maluku, Indonesia. IOP Conf. Ser. Earth Environ. Sci. 339, 012003 (2019).Article 

    Google Scholar 
    27.Horwitz, R., Hoogenboom, M. O. & Fine, M. Spatial competition dynamics between reef corals under ocean acidification. Sci. Rep. 7, 40288 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Noonan, S. H. C., Fabricius, K. E. & Humphrey, C. Symbiodinium community composition in scleractinian corals is not affected by life-long exposure to elevated carbon dioxide. PLoS ONE 8, e63985 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Caroselli, E. et al. Environmental implications of skeletal micro-density and porosity variation in two scleractinian corals. Zoology 114, 255–264 (2011).PubMed 
    Article 

    Google Scholar 
    30.Reggi, M. et al. Biomineralization in Mediterranean corals: The role of the intraskeletal organic matrix. Cryst. Growth Des. 14, 4310–4320 (2014).CAS 
    Article 

    Google Scholar 
    31.Goffredo, S. et al. The skeletal organic matrix from Mediterranean coral Balanophyllia Europaea influences calcium carbonate precipitation. PLoS ONE 6, e22338 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Goffredo, S. et al. Biomineralization control related to population density under ocean acidification. Nat. Clim. Chang. 4, 593–597 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Borgia, G. C., Brown, R. J. S. & Fantazzini, P. Uniform-penalty inversion of multiexponential decay data. J. Magn. Reson. 132, 65–77 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    34.Bortolotti, F., Brown, R. & Fantazzini, P. UpenWin: A Software for Inversion of Multiexponential Decay Data (Windows System Alma Mater Studiorum—Università di Bologna, 2012).
    Google Scholar 
    35.Fantazzini, P. et al. A time-domain nuclear magnetic resonance study of Mediterranean scleractinian corals reveals skeletal-porosity sensitivity to environmental changes. Environ. Sci. Technol. 47, 12679–12686 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Coronado, I., Fine, M., Bosellini, F. R. & Stolarski, J. Impact of ocean acidification on crystallographic vital effect of the coral skeleton. Nat. Commun. 10, 2896 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Pokroy, B., Fitch, A. & Zolotoyabko, E. The microstructure of biogenic calcite: A view by high-resolution synchrotron powder diffraction. Adv. Mater. 18, 2363–2368 (2006).CAS 
    Article 

    Google Scholar 
    38.Anderson, M. J., Gorley, R. N. & Clarke, K. R. PERMANOVA+ for PRIMER: Guide to software and statistical methods. In Plymouth (2008).39.R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018). ISBN 3-900051-07-0. http://www.R-project.org.40.Toby, B. H. & Von Dreele, R. B. GSAS-II: The genesis of a modern open-source all purpose crystallography software package. J. Appl. Crystallogr. 46, 544–549 (2013).CAS 
    Article 

    Google Scholar 
    41.Jiang, H. G., Rühle, M. & Lavernia, E. J. On the applicability of the x-ray diffraction line profile analysis in extracting grain size and microstrain in nanocrystalline materials. J. Mater. Res. 14, 549–559 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    42.Vercelloni, J. et al. Forecasting intensifying disturbance effects on coral reefs. Glob. Chang. Biol. 26, 2785–2797 (2020).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Guo, W. et al. Ocean acidification has impacted coral growth on the Great Barrier Reef. Geophys. Res. Lett. 47, 1–9 (2020).
    Google Scholar 
    44.Tambutté, E. et al. Morphological plasticity of the coral skeleton under CO2-driven seawater acidification. Nat. Commun. 6, 7368 (2015).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    45.Schneider, K. & Erez, J. The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol. Oceanogr. 51, 1284–1293 (2006).ADS 
    CAS 
    Article 

    Google Scholar 
    46.Martinez, A. et al. Species-specific calcification response of Caribbean corals after 2-year transplantation to a low aragonite saturation submarine spring. Proc. Biol. Sci. 286, 20190572 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Comeau, S. et al. Resistance to ocean acidification in coral reef taxa is not gained by acclimatization. Nat. Clim. Chang. 9, 477–483 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    48.McCulloch, M. et al. Resilience of cold-water scleractinian corals to ocean acidification: Boron isotopic systematics of pH and saturation state up-regulation. Geochim. Cosmochim. Acta 87, 21–34 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    49.Movilla, J. et al. Differential response of two Mediterranean cold-water coral species to ocean acidification. Coral Reefs 33, 675–686 (2014).ADS 
    Article 

    Google Scholar 
    50.Kurihara, H., Takahashi, A., Reyes-Bermudez, A. & Hidaka, M. Intraspecific variation in the response of the scleractinian coral Acropora digitifera to ocean acidification. Mar. Biol. 165, 38 (2018).Article 

    Google Scholar 
    51.Barnes, D. J. & Devereux, M. J. Variations in skeletal architecture associated with density banding in the hard coral Porites. J. Exp. Mar. Biol. Ecol. 121, 37–54 (1988).Article 

    Google Scholar 
    52.Bucher, D. J., Harriott, V. J. & Roberts, L. G. Skeletal micro-density, porosity and bulk density of acroporid corals. J. Exp. Mar. Biol. Ecol. 228, 117–136 (1998).Article 

    Google Scholar 
    53.Mass, T. et al. Amorphous calcium carbonate particles form coral skeletons. Proc. Natl. Acad. Sci. 114, E7670–E7678 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Vidal-Dupiol, J. et al. Genes related to ion-transport and energy production are upregulated in response to CO2-driven pH decrease in corals: New insights from transcriptome analysis. PLoS ONE 8, e58652 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Suggett, D. J. et al. Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32, 327–337 (2013).ADS 
    Article 

    Google Scholar 
    56.Vogel, N., Meyer, F., Wild, C. & Uthicke, S. Decreased light availability can amplify negative impacts of ocean acidification on calcifying coral reef organisms. Mar. Ecol. Prog. Ser. 521, 49–61 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    57.Tanaka, Y. et al. Nutrient availability affects the response of juvenile corals and the endosymbionts to ocean acidification. Limnol. Oceanogr. 59, 1468–1476 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    58.Towle, E. K., Enochs, I. C. & Langdon, C. Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS ONE 10, e0123394 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    59.Stolarski, J., Przeniosło, R., Mazur, M. & Brunelli, M. High-resolution synchrotron radiation studies on natural and thermally annealed scleractinian coral biominerals. J. Appl. Crystallogr. 40, 2–9 (2007).CAS 
    Article 

    Google Scholar 
    60.Maslen, E. N., Streltsov, V. A., Streltsova, N. R. & Ishizawa, N. Electron density and optical anisotropy in rhombohedral carbonates. III. Synchrotron X-ray studies of CaCO3, MgCO3 and MnCO3. Acta Crystallogr. Sect. B Struct. Sci. 51, 929–939 (1995).Article 

    Google Scholar 
    61.Wall, M. et al. Linking internal carbonate chemistry regulation and calcification in corals growing at a Mediterranean CO2 vent. Front. Mar. Sci. 6, 699 (2019).Article 

    Google Scholar 
    62.Wickham, H. ggplot2 (Springer International Publishing, 2016). https://doi.org/10.1007/978-3-319-24277-4.Book 
    MATH 

    Google Scholar  More