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    Deep-sea bacteria trigger settlement and metamorphosis of the mussel Mytilus coruscus larvae

    1.
    Liang, X., Liu, Y. Z., Chen, K., Li, Y. F. & Yang, J. L. Identification of MyD88-4 in Mytilus coruscus and expression changes in response to Vibrio chagasii challenge (in Chinese with English abstract). J. Fish. China. 43, 2347–2358 (2019).
    Google Scholar 
    2.
    Li, T. W. Marine Biology (in Chinese) (China Ocean Press, Beijing, 2013).
    Google Scholar 

    3.
    Liang, X. et al. Effects of dynamic succession of Vibrio biofilms on settlement of the mussel Mytilus coruscus (in Chinese with English abstract). J. Fish. China. 44, 118–129 (2020).
    Google Scholar 

    4.
    Whalan, S. & Webster, N. S. Sponge larval settlement cues: the role of microbial biofilms in a warming ocean. Sci. Rep. 4, 4072 (2014).
    ADS  CAS  Article  Google Scholar 

    5.
    Satuito, C. G., Natoyama, K., Yamazaki, M. & Fusetani, N. Induction of attachment and metamorphosis of laboratory cultured mussel Mytilus edulis galloprovincialis larvae by microbial film. Fish. Sci. 61, 223–227 (1995).
    CAS  Article  Google Scholar 

    6.
    Zhao, B., Zhang, S. & Qian, P. Y. Larval settlement of the silver-or goldlip pearl oyster Pinctada maxima (Jameson) in response to natural biofilms and chemical cues. Aquaculture 220, 883–901 (2003).
    Article  Google Scholar 

    7.
    Rahim, S. A. K. A., Li, J. Y. & Kitamura, H. Larval metamorphosis of the sea urchins, Pseudocentrotus depressus and Anthocidaris crassispina in response to microbial film. Mar. Biol. 144, 71–78 (2004).
    Article  Google Scholar 

    8.
    Bao, W. Y., Satuito, C. G., Yang, J. L. & Kitamura, H. Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Mar. Biol. 150, 565–574 (2007).
    Article  Google Scholar 

    9.
    Huang, Y., Callahan, S. & Hadfield, M. G. Recruitment in the sea: bacterial genes required for inducing larval settlement in a polychaete worm. Sci. Rep. 2, 228 (2012).
    ADS  Article  Google Scholar 

    10.
    Wang, C. et al. Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to natural biofilms. Biofouling 28, 249–256 (2012).
    Article  Google Scholar 

    11.
    Yang, J. L. et al. Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 29, 247–259 (2013).
    CAS  Article  Google Scholar 

    12.
    Liang, X. et al. The flagellar gene regulates biofilm formation and mussel larval settlement and metamorphosis. Int. J. Mol. Sci. 21, 710 (2020).
    CAS  Article  Google Scholar 

    13.
    Peng, L. H., Liang, X., Xu, J. K., Dobretsov, S. & Yang, J. L. Monospecific biofilms of Pseudoalteromonas promote larval settlement and metamorphosis of Mytilus coruscus. Sci. Rep. 10, 2577 (2020).
    ADS  CAS  Article  Google Scholar 

    14.
    Schippers, A. et al. Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria. Nature 433, 861–864 (2005).
    ADS  CAS  Article  Google Scholar 

    15.
    Orcutt, B. N., Sylvan, J. B., Knab, N. J. & Edwards, K. J. Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol. Mol. Biol. Rev. 75, 361–422 (2011).
    CAS  Article  Google Scholar 

    16.
    Woodall, L. C. et al. Deep-sea anthropogenic macrodebris harbours rich and diverse communities of bacteria and archaea. PLoS ONE 13, e0206220 (2018).
    Article  Google Scholar 

    17.
    Wieczorek, S. K. & Todd, C. D. Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12, 81–118 (1998).
    Article  Google Scholar 

    18.
    Qian, P. Y., Lau, S. C. K., Dahms, H. U., Dobretsov, S. & Harder, T. Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar. Biotechnol. 9, 399–410 (2007).
    CAS  Article  Google Scholar 

    19.
    Dobretsov, S. in Marine and Industrial Biofouling (eds Flemming, H. C. et al.) 293–313 (Springer, 2009).

    20.
    Huang, S. & Hadfield, M. G. Composition and density of bacterial biofilms determine larval settlement of the polychaete Hydroides elegans. Mar. Ecol. Prog. Ser. 260, 161–172 (2003).
    ADS  CAS  Article  Google Scholar 

    21.
    Tran, C. & Hadfield, M. G. Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Mar. Ecol. Prog. Ser. 433, 85–96 (2011).
    ADS  Article  Google Scholar 

    22.
    Dahms, H. U., Dobretsov, S. & Qian, P. Y. The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J. Exp. Mar. Biol. Ecol. 313, 191–209 (2004).
    Article  Google Scholar 

    23.
    Lau, S. C. K., Thiyagarajan, V. & Qian, P. Y. The bioactivity of bacterial isolates in Hong Kong waters for the inhibition of barnacle (Balanus amphitrite Darwin) settlement. J. Exp. Mar. Biol. Ecol. 282, 43–60 (2003).
    Article  Google Scholar 

    24.
    Lau, S. C. K. & Qian, P. Y. Larval settlement in the serpulid polychaete Hydroides elegans in response to bacterial films: an investigation of the nature of putative larval settlement cue. Mar. Biol. 138, 321–328 (2001).
    Article  Google Scholar 

    25.
    Bao, W. Y., Yang, J. L., Satuito, C. G. & Kitamura, H. Larval metamorphosis of the mussel Mytilus galloprovincialis in response to Alteromonas sp. 1: evidence for two chemical cues?. Mar. Biol. 152, 657–666 (2007).
    Article  Google Scholar 

    26.
    Unabia, C. R. C. & Hadfield, M. G. Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar. Biol. 133, 55–64 (1999).
    Article  Google Scholar 

    27.
    Hadfield, M. G. Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu. Rev. Mar. Sci. 3, 453–470 (2011).
    ADS  Article  Google Scholar 

    28.
    Flemming, H. C. & Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 8, 623–633 (2010).
    CAS  Article  Google Scholar 

    29.
    Flemming, H. C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).
    CAS  Article  Google Scholar 

    30.
    Karygianni, L., Ren, Z., Koo, H. & Thurnheer, T. Biofilm matrixome: extracellular components in structured microbial communities. Trends Microbiol. 28, 668–681 (2020).
    CAS  Article  Google Scholar 

    31.
    Fulaz, S., Vitale, S., Quinn, L. & Casey, E. Nanoparticle–biofilm interactions: the role of the EPS matrix. Trends Microbiol. 27, 915–926 (2019).
    CAS  Article  Google Scholar 

    32.
    Dragoš, A. & Kovács, Á. T. The peculiar functions of the bacterial extracellular matrix. Trends Microbiol. 25, 257–266 (2017).
    Article  Google Scholar 

    33.
    Mayer, C. et al. The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int. J. Biol. Macromol. 26, 3–16 (1999).
    CAS  Article  Google Scholar 

    34.
    Liang, X. et al. Effects of biofilms of deep-sea bacteria under varying temperatures on larval metamorphosis of Mytilus coruscus (in Chinese with English abstract). J. Fish. China. 44, 131–144 (2020).
    Google Scholar 

    35.
    Huggett, M. J., Williamson, J. E., de Nys, R., Kjelleberg, S. & Steinberg, P. D. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149, 604–619 (2006).
    ADS  Article  Google Scholar 

    36.
    Yang, J. L., Satuito, C. G., Bao, W. Y. & Kitamura, H. Induction of metamorphosis of pediveliger larvae of the mussel Mytilus galloprovincialis Lamarck, 1819 using neuroactive compounds, KCl, NH4Cl and organic solvents. Biofouling 24, 461–470 (2008).
    CAS  Article  Google Scholar 

    37.
    Yang, J. L., Li, Y. F., Bao, W. Y., Satuito, C. G. & Kitamura, H. Larval metamorphosis of the mussel Mytilus galloprovincialis Lamarck, 1819 in response to neurotransmitter blockers and tetraethylammonium. Biofouling 27, 193–199 (2011).
    CAS  Article  Google Scholar 

    38.
    Yang, J. L., Satuito, C. G., Bao, W. Y. & Kitamura, H. Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis on different macroalgae. Mar. Biol. 152, 1121–1132 (2007).
    Article  Google Scholar 

    39.
    Bao, W. Y., Lee, O. O., Chung, H. C., Li, M. & Qian, P. Y. Copper affects biofilm inductiveness to larval settlement of the serpulid polychaete Hydroides elegans (Haswell). Biofouling 26, 119–128 (2009).
    Article  Google Scholar 

    40.
    Peng, L. H. et al. A bacterial polysaccharide biosynthesis-related gene inversely regulates larval settlement and metamorphosis of Mytilus coruscus. Biofouling 36, 753–765 (2020).
    CAS  Article  Google Scholar  More

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    Modeling of trees failure under windstorm in harvested Hyrcanian forests using machine learning techniques

    Site selection
    Hyrcanian temperate forests, dominated by old broadleaf trees, are located in the north of Iran adjacent to the Caspian Sea. We selected the Neka Zalemroud forest in Mazandaran province as the study area for this research (36° 26′ 09″ to 36° 30′ 47″ N latitude and 53° 20′ 34″ to 53° 31′ 51″ E longitude) as the boundaries of sampling area have been illustrated in Fig. 1 by the authors. This forest has been covered with 2533 hectares of old broadleaf trees such as Fagus orientalis, Carpinus betulus, Quercus castanafolia, Acer velutinum, Acer cappadocicum, Parrotia persica and some other species. This region is affected by permanent winds and the maximum wind speed is in the range of 10 to  > 30 m/s. The windstorms with more than 100 km/h cause damage forest trees, including uprooting or stem breakage. The windstorms cause many tree failures annually, which is in result of the tree harvesting and gap creation in forest stands. Hence, we aimed to identify the uprooted or stem broken trees using the sample plots data after the windstorm with 100 km/h (4 h) on 21 March 2018.
    Figure 1

    The location of study area and sample plots (QGIS 3.12.0, https://www.qgis.org/en/site/).

    Full size image

    Methods
    Data from field measurement of 600 sample plots in the study area were summarized before and after the windstorm in March 2018. ARC MAP 9.3 software was used to spatially locate the sample plots on the forest map. Also, the slope of plots was defined by topography map (1:50,000) in this software. The permanent sample plots were created by Department of Natural Resources of Mazandaran Province (in the structure of the forest management plan) as a part of government-sponsored “permanent sample plot” protocol to monitor the changes in the number of trees and species48. In this protocol, the centers of these sample plots are marked with a metal rod and the geographical coordinates are recorded. The attributes of all trees in the sample plots are recorded consisting of species, diameter at the breast height, tree’s height, number of trees, distance to the center of the plot, crown diameter and land, soil and climate characteristics of the plot location. On average, in each plot, there are about 10 to 20 trees with a diameter of more than 7 cm (marketable size), and using the recorded data of the trees, it is possible to identify each tree in subsequent monitoring. As the protocol dictates, preliminary data were recorded on the stage of creating plots by experts from the Provincial Department of Natural Resources in 201649. After the windstorm on 21 March 2018, these plots were investigated by the authors to find damaged and undamaged trees. The area of each sample plot was 1000 m2 and in the shape of the circle with 17.84 m radius. These plots were investigated to record harmed trees which were uprooted or stem broken. Sample plots are clustered into susceptible (with harmed trees) and unsusceptible (without harmed trees) plots. We recorded the forest stand attributes, as well as tree attributes, which influence the likelihood of trees to be damaged in windstorms. Therefore, we investigate the damaged and resistant trees in the plots within 1000 m2 area. The stand variables were recorded in the plot area such as the mean of the trees’ height in the plot. Some plots (306 plots) were determined where the damaged trees were observed and some others (294 plots) were determined where the target tree in the middle of the plot was undisturbed. In a literature review, we found that stand and tree characteristics influence wind-susceptibility of trees (such as tree diameter and height, spread crown area, rooting system, soil type, stand density, topography, etc.1,3,19,20,21). Therefore, 15 variables in 600 sample plots were recorded that are divided into two categories: 1. Forest stand variables: Plot Slope (PS) (%), Soil Depth (SD) in plot area (cm), trees Mean Diameter at the Breast Height (MDBH) at plot (cm), trees Mean Height (MH) in plot (m), trees Density (De) in plot (Number of trees), trees Diversity (Di) in plot (Number of tree species), Number of Thicker trees in diameter (than the target tree) (NTh), and Number of Taller trees (than the target tree) (NTa).
    2.Tree variables (bigger than marketable size): Tree Area (TA) (occupied area by the tree) (m2), Tree Diameter at the Breast Height (TDBH) (cm), Tree Height (TH) (m), Tree Crown Diameter (TCD) (m), Mean Distance from Neighbor trees (MeDN) (m), Minimum Distance from Neighbor trees (MiDN) (m), and Maximum Distance from Neighbor trees (MaDN) (m). Tree heights and some more data were recorded in permanent sample plots before the windstorm. Therefore, we used the recorded data at the stage of creating plots, for damaged trees. In fact, 10 to 20 trees are recorded in each plot and using the recorded data of the trees (species, diameter, distance to the center of the plot, etc.) it is possible to identify target trees (damaged or undamaged) in subsequent monitoring. There are some other factors that influence wind-susceptibility of trees such as forest edge, tree diversity, and land form. In this research, we were looking for the impact of forest plan activities on tree failure; therefore, we neutralized forest edge effects by selecting sample plots inside the forest stands which are far from the forest edges. In land form variables, land slope was considered in stand variables, but altitude and geographical aspect of the hill, as well as tree diversity, were omitted because of limited variation in the samples.
    Tree Failure Model (TFM) was developed by recording 15 variables of the trees and forest stands in 600 selected sample plots. In fact, we designed three TFMs with three modeling techniques to achieve the most accurate one based on model accuracy assessment. The damaged trees in the plots were identified by two features: (1) The tree was uprooted by wind forces along the windstorm. (2) The tree was uprooted or stem broken. Leaning trees (under windstorm force) were also counted as uprooted trees. The damaged tree was chosen as the target tree in susceptible plots (plots with a damaged tree). Also, the central tree was selected as the target tree in the wind-unsusceptible plots (plots without damaged tree). Indeed, the output of TFM will be in two classes of damaged trees (1) and stable trees (0). Hence, the response or output of the model will be a discrete class {0,1}. The accuracy of the model is assessed by confusion matrices which detect the number of accurate and false classifications of sample trees.
    The new mathematical modeling approaches and machine learning techniques are needed to cover limitation in data collection and forest inventories. Indeed, ANNs are over 50 years old, but just not often applied yet. History of ANN development represents this fact that learning algorithms and structure of neural networks are developed every year. Therefore, we developed artificial intelligence techniques in natural phenomena modeling11,17 namely MLP, RBFNN, and SVM.
    Machine learning techniques rely on a specific concept that is “a set of weak learners develop a single strong learner” (by Freund and Schapire22, Breiman23 and Breiman et al.24). As it is known, a weak learner is a classifier correlating slightly with the real (target) classification; while a strong learner is well correlated with real (target) classification. Machine learning algorithms are trying to combine weak classification rules in a one strong classification rule. Based on this approach, we used 15 variables (even if we believe that these variables are not related to tree susceptibility in the wind) and tested some algorithms and variable weights to make weak learners or rules and combining them into one strong rule in the structure of three machine learning techniques.
    Multi-layer perceptron (MLP) neural network
    ANNs use different methods, such as feed-forward, backward, recurrent and other, to teach the network for output prediction. MLP is a multi-layer form of Feed-forward neural networks without any cycle or loop. In Feed-forward neural networks, the information analysis is performed in one direction from the input layer, through the hidden layer to the output layer47. In this learning method, the errors of the network propagate from the output layer to inputs to revise the weights of input variables. MLP is a multi-layer Artificial Neural Network (ANN) model with self-learning mechanism which uses samples for classification. Indeed, MLP has been using some interconnected processing elements that are called PEs (Processing Elements). MLP learns by using samples and transfer functions which are applied between neurons and hidden layers in a computer program17. In the training process, each PE receives signals periodically from other PEs and sends the new signal to other processors. Considering inputs, MLP adjusts the weights of neurons continuously, and the learning process is completed.
    We used some activation functions (such as logarithmic sigmoid, hyperbolic tangent, and linear transfer functions) which determine the relation between inputs and outputs and these functions were tested to achieve the best performance of MLP. Back Propagation (BP) method propagates the error of outputs to the input layer where the first random weights have been assigned. The weights of the network inputs will be justified until the best performance of the network is reached; and after that, the learning process will be completed7,11. Errors between Ynet (MLP output) and Y (real class of tree failure) are decreased by BP when the weight of neurons or Processing Elements (PEs) (w) and input variables (x) come to the best performance, and the output of jth PE on the kth layer (PEkj) will be achieved by Eq. (1):

    $$net_{j}^{k} = mathop sum limits_{i = 0}^{n} w_{ji} x_{ji}$$
    (1)

    Transfer functions are used in the structure of network, and neuron output value is determined by (Eq. 2).

    $$Y_{net} = smallint net_{j}$$
    (2)

    Finally, weights of t samples will be adjusted by delta rule which has been summarized in Eq. (3).

    $$w_{ji}^{t} = w_{ji}^{t – 1} + Delta w_{ji}^{t}$$
    (3)

    By using the ANN function in MATLAB R2013b, 360 uniformly distributed random samples (60% of 600 samples) were defined as training data set. 120 evenly distributed random samples (20% of 600 samples) were defined as validation data set, and 120 samples (20% of 600 samples) were determined as test data set. All data were normalized to the interval of 0 to 1 using the Min–Max technique by mapminmax function in MATLAB R2013b (Refer to Demuth and Beale25 for MATLAB codes for MLP neural network development and related preprocessing algorithms).
    Radial basis function neural network (RBFNN)
    Radial basis function neural network is architecturally similar to the MLP with different activation function in the hidden layer. RBFNNs have been used in function approximation and classification in researches of the last decade13,26,27,28. RBFNN uses samples in two data sets of training and test. The radial function is applied in each neuron of the hidden layer; and the number of neurons depends on input matrix of variables. Considering two classes of trees failure (0 and 1) in this research, we have two output layers in the structure of RBFNN. Gaussian function is the most frequently used function in the hidden layers of RBFNN13,27. The Gaussian function can find the center of circular classifiers successfully. The Gaussian function regulates the centre of mentioned circular classifiers by Eq. (4).

    $$R_{j} left( x right) = expleft( {frac{{||x – a_{j} ||^{2} }}{{2sigma^{2} }}} right)$$
    (4)

    In Eq. (4), input variables are structured in the matrix “x”, radial basis function has been defined as Rj(x), centre of RBF function is presented as aj, and we have a positive real number as “ϭ”. The outputs of network will be calculated by an output function Eq. (5).

    $$y_{k} = mathop sum limits_{j = 1}^{m} w_{jk} R_{j} left( x right) + b_{j}$$
    (5)

    In Eq. (5), the number of calculation nodes in the structure of hidden layers (j), the number of neurons (m), the weights of neurons (wik), and a bias value (bj) have been used to calculate output (yk).
    Neuron weights (wjk) are updated continuously to decrease output errors until network training process comes to end. Network performance is calculated when the number of neurons and the weights of neuron or layers are fixed13. (Refer to Demuth and Beale25 for MATLAB codes for RBF neural network development and related preprocessing algorithms).
    Support vector machine (SVM)
    SVM is one of the machine learning techniques that requires quite a lot of data for training, but this method also provides more accurate results than other methods when the volume of training data is limited29,30. Therefore, SVM has been used for modeling in this paper to deal with this issue with the collected data along forest inventory.
    As a classifier technique, SVM aims to determine the largest margin in decision boundaries that could separate classes of decision31. SVM is looking for the largest margin in the boundaries of classification when the uncertainties in the decision are expected27. This method of prediction minimizes the probability of over-fitting in classes limits of tree failure.
    We have two datasets of training and test in the structure of SVM. The values of target are structured in a n-dimensional matrix so it is possible to find the most accurate boundaries and margins. Equation (6) is the SVM model and equation parameters define: y(x) = SVM output, α_i = a multiplier, K = kernel function, and b = threshold parameter.

    $$yleft( x right) = mathop sum limits_{i = 1}^{n} alpha_{i} Kleft( {x_{i} ,x_{j} } right) + b$$
    (6)

    Then we defined Gaussian Radial Basis Function (RBF) in Eq. (7), in the context of non-linear SVM. As we know, RBF is the most popular function in the context of SVM with remarkable ability to control generalization of SVM classifier.

    $$Kleft( {x_{i} ,x_{j} } right) = {text{exp}}left( { – gamma| x_{i} – x_{j}|^{2} } right)$$
    (7)

    The parameters of Eq. (7) are: xi and xj = samples and γ = kernel parameter.
    Finally, primal problem in Eq. (8) should be minimized to achieve the most accurate SVM for tree failure prediction.

    $$frac{1}{2}|w|^{2} + Cmathop sum limits_{i = 1}^{n} xi_{i}$$
    (8)

    In Eq. (8), the parameters are: 1/2||w||2 = the margin, Σξi = training errors and C = the tuning parameter.
    SVM uses samples in two data sets of training and test. The classes of the target will be summarized in a n-dimensional matrix to determine the nearest classification boundaries and margins. (Refer to Demuth and Beale25 for MATLAB codes for SVM neural network development and related preprocessing algorithms).
    Model selection
    MLP, RBFNN, and SVM models were run on the training dataset with 15 tree variables as inputs and tree failure classes in 600 selected trees as output. To evaluate prediction accuracy of the MLP, RBFNN, and SVM models, we used the confusion matrix to determine the percentage of accuracy in target tree classification. Also, the number of trees with accurate and failed classification will be detected11.
    Sensitivity analysis
    Sensitivity analysis was designed to prioritize the most accurate model variables with respect to the significance of variables in output. Sensitivity analysis defines the usefulness of variables in model predictions. In sensitivity analysis, we changed each variable in the range of standard deviation with 50 steps while the other variables were fixed at the value of the average. Then, the standard deviation of outputs for each variable changes was measured as model sensitivity for that variable. Variables with high value in the outputs standard deviation are the most important variables with more influence on model outputs. The trend of model output changes with changing the most significant variables, in the range of standard deviation (50 steps) was illustrated in some figures to find out the way that model outputs are changing with variable changes (negatively or positively) (Refer to Kalantary et al.27 and Jahani et al.13.
    Environmental decision support system (EDSS) tool
    Finally a user friendly GUI (Graphical User Interface) tool was designed as an EDSS for susceptible tree identification in windstorms. It is applicable for forest managers who are looking for hazardous trees to plan for tree protection and increase the forest stands resistant against windstorms. ANN models use a huge matrix of weights; so model execution should be in the mathematical software (in this research MATLAB R2013b). Users, who are not familiar with the software, need a simple tool to run the model on new samples and get the results of prediction. To design EDSS tool, we developed a GUI extension in MATLAB R2013b software. With this tool, users enter the values of trees and stands variables (based on forest inventory data in other target forests) and the susceptible trees will be identified only by pushing a button. The model will be run on the data and the model outputs for each tree will be appeared in a table (0 or 1). More

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    Effect of temperature on the unimodal size scaling of phytoplankton growth

    1.
    Finkel, Z. V. et al. Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32, 119–137 (2010).
    CAS  Article  Google Scholar 
    2.
    Marañón, E. Cell size as a key determinant of phytoplankton metabolism and community structure. Ann. Rev. Mar. Sci. 7, 241–264 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    3.
    Chavez, F. P., Messié, M. & Pennington, J. T. marine primary production in relation to climate variability and change. Ann. Rev. Mar. Sci. 3, 227–260 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    4.
    Kleiber, M. Body size and metabolism. Hilgardia J. Agric. Sci. 6, 315–353 (1932).
    CAS  Article  Google Scholar 

    5.
    Gillooly, J. F. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).
    Article  Google Scholar 

    7.
    Raven, J. A. Why are there no picoplanktonic O2 evolvers with volumes less than 10–19 m3?. J. Plankton Res. 16, 565–580 (1994).
    Article  Google Scholar 

    8.
    Bec, B., Collos, Y., Vaquer, A., Mouillot, D. & Souchu, P. Growth rate peaks at intermediate cell size in marine photosynthetic picoeukaryotes. Limnol. Oceanogr. 53, 863–867 (2008).
    ADS  Article  Google Scholar 

    9.
    Chen, B. & Liu, H. Relationships between phytoplankton growth and cell size in surface oceans: interactive effects of temperature, nutrients, and grazing. Limnol. Oceanogr. 55, 965–972 (2010).
    ADS  CAS  Article  Google Scholar 

    10.
    Marañón, E. et al. Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use. Ecol. Lett. 16, 371–379 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    11.
    Ward, B. A., Marañón, E., Sauterey, B., Rault, J. & Claessen, D. The size dependence of phytoplankton growth rates: a trade-off between nutrient uptake and metabolism. Am. Nat. 189, 170–177 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    12.
    Chen, B., Liu, H., Huang, B. & Wang, J. Temperature effects on the growth rate of marine picoplankton. Mar. Ecol. Prog. Ser. 505, 37–47 (2014).
    ADS  Article  Google Scholar 

    13.
    Sal, S., Alonso-Saez, L., Bueno, J., Garcıa, F. C. & Lopez-Urrutia, A. Thermal adaptation, phylogeny, and the unimodal size scaling of marine phytoplankton growth. Limnol. Oceanogr. 60, 1212–1221 (2015).
    ADS  Article  Google Scholar 

    14.
    Bissinger, J. E., Montagnes, D. J. S., Sharples, J. & Atkinson, D. Predicting marine phytoplankton maximum growth rates from temperature: improving on the Eppley curve using quantile regression. Limnol. Oceanogr. 53, 487–493 (2008).
    ADS  Article  Google Scholar 

    15.
    Chen, B. Patterns of thermal limits of phytoplankton. J. Plankton Res. 37, 285–292 (2015).
    Article  Google Scholar 

    16.
    Thomas, M. K., Kremer, C. T. & Litchman, E. Environment and evolutionary history determine the global biogeography of phytoplankton temperature traits. Glob. Ecol. Biogeogr. 25, 75–86 (2016).
    Article  Google Scholar 

    17.
    Heinle, M. The effects of light, temperature and nutrients on coccolithophores and implications for biogeochemical models (Doctoral dissertation, University of East Anglia, Norwich, United Kingdom). (2013).

    18.
    Kruskopf, M. & Flynn, K. J. Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol. 169, 841–842 (2006).
    Article  CAS  Google Scholar 

    19.
    Flynn, K. J. & Raven, J. A. What is the limit for photoautotrophic plankton growth rates?. J. Plankton Res. 39, 13–22 (2016).
    Article  CAS  Google Scholar 

    20.
    Prakash, A., Skoglund, L., Rystad, B. & Jensen, A. Growth and cell-size distribution of marine planktonic algae in batch and dialysis cultures. J. Fish. Res. Board Canada 30, 143–155 (1973).
    Article  Google Scholar 

    21.
    Xia, L., Huang, R., Li, Y. & Song, S. The effect of growth phase on the surface properties of three oleaginous microalgae (Botryococcus sp. FACGB-762, Chlorella sp. XJ-445 and Desmodesmus bijugatus XJ-231). PLoS ONE 12, e0186434 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    22.
    Verdy, A., Follows, M. & Flierl, G. Optimal phytoplankton cell size in an allometric model. Mar. Ecol. Prog. Ser. 379, 1–12 (2009).
    ADS  Article  Google Scholar 

    23.
    Kempes, C. P., Dutkiewicz, S. & Follows, M. J. Growth, metabolic partitioning, and the size of microorganisms. Proc. Natl. Acad. Sci. U.S.A. 109, 495–500 (2012).
    ADS  CAS  PubMed  Article  Google Scholar 

    24.
    Stawiarski, B., Buitenhuis, E. T. & Quéré, C. L. The physiological response of picophytoplankton to temperature and its model representation. Front. Mar. Sci. 3, 1–13 (2016).
    Article  Google Scholar 

    25.
    Martiny, A. C., Ma, L., Mouginot, C., Chandler, J. W. & Zinser, E. R. Interactions between thermal acclimation, growth rate, and phylogeny influence prochlorococcus elemental stoichiometry. PLoS ONE 11, 1–12 (2016).
    Article  CAS  Google Scholar 

    26.
    Mackey, K. R. M. et al. Effect of temperature on photosynthesis and growth in marine Synechococcus spp. Plant Physiol. 163, 815–829 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    27.
    Demory, D. et al. Picoeukaryotes of the Micromonas genus: sentinels of a warming ocean. ISME J. 13, 132–146 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    28.
    Pittera, J. et al. Connecting thermal physiology and latitudinal niche partitioning in marine Synechococcus. ISME J. 8, 1221–1236 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    29.
    Barton, S. & Yvon-Durocher, G. Quantifying the temperature dependence of growth rate in marine phytoplankton within and across species. Limnol. Oceanogr. 64, 2081–2091 (2019).
    ADS  Article  Google Scholar 

    30.
    Kremer, C. T., Thomas, M. K. & Litchman, E. Temperature- and size-scaling of phytoplankton population growth rates: reconciling the Eppley curve and the metabolic theory of ecology. Limnol. Oceanogr. 62, 1658–1670 (2017).
    ADS  Article  Google Scholar 

    31.
    Berthelot, H. et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 13, 651–662 (2019).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    32.
    Duhamel, S., Kim, E., Sprung, B. & Anderson, O. R. Small pigmented eukaryotes play a major role in carbon cycling in the P-depleted western subtropical North Atlantic, which may be supported by mixotrophy. Limnol. Oceanogr. 64, 2424–2440 (2019).
    ADS  CAS  Article  Google Scholar 

    33.
    Worden, A. Z., Nolan, J. K. & Palenik, B. Assessing the dynamics and ecology of marine picophytoplankton: the importance of the eukaryotic component. Limnol. Oceanogr. 49, 168–179 (2004).
    ADS  CAS  Article  Google Scholar 

    34.
    Gutierrez-Rodríguez, A., Selph, K. E. & Landry, M. R. Phytoplankton growth and microzooplankton grazing dynamics across vertical environmental gradients determined by transplant in situ dilution experiments. J. Plankton Res. 38, 271–289 (2015).
    PubMed  PubMed Central  Article  Google Scholar 

    35.
    Worden, A. Z. & Binder, B. J. Application of dilution experiments for measuring growth and mortality rates among Prochlorococcus and Synechococcus populations in oligotrophic environments. Aquat. Microb. Ecol. 30, 159–174 (2003).
    Article  Google Scholar 

    36.
    DeLong, J. P., Okie, J. G., Moses, M. E., Sibly, R. M. & Brown, J. H. Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proc. Natl. Acad. Sci. U.S. A. 107, 12941–12945 (2010).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    37.
    García, F. C. et al. The allometry of the smallest: superlinear scaling of microbial metabolic rates in the Atlantic Ocean. ISME J. 10, 1029–1036 (2016).
    PubMed  Article  CAS  Google Scholar 

    38.
    Kiørboe, T. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv. Mar. Biol. 29, 1–72 (1993).
    Article  Google Scholar 

    39.
    Marãnón, E. et al. Resource supply overrides temperature as a controlling factor of marine phytoplankton growth. PLoS ONE 9, 20–23 (2014).
    Article  CAS  Google Scholar 

    40.
    Behrenfeld, M. J., Boss, E., Siegel, D. A. & Shea, D. M. Carbon-based ocean productivity and phytoplankton physiology from space. Global Biogeochem. Cycles 19, 1–14 (2005).
    Article  CAS  Google Scholar 

    41.
    Tsuda, A. et al. A mesoscale iron enrichment in the Western subarctic Pacific induces a large centric diatom bloom. Science 300, 958–961 (2003).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    42.
    Latasa, M., Landry, M. R., Schlüter, L. & Bidigare, R. R. Pigment-specific growth and grazing rates of phytoplankton in the central equatorial pacific. Limnol. Oceanogr. 42, 289–298 (1997).
    ADS  CAS  Article  Google Scholar 

    43.
    Cavender-Bares, K. K., Mann, E. L., Chisholm, S. W., Ondrusek, M. E. & Bidigare, R. R. Differential response of equatorial Pacific phytoplankton to iron fertilization. Limnol. Oceanogr. 44, 237–246 (1999).
    ADS  CAS  Article  Google Scholar 

    44.
    Mouriño-Carballido, B. et al. Nutrient supply controls picoplankton community structure during three contrasting seasons in the northwestern Mediterranean Sea. Mar. Ecol. Prog. Ser. 543, 1–19 (2016).
    ADS  Article  CAS  Google Scholar 

    45.
    Schmidt, K. et al. Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation. Glob. Chang. Biol. https://doi.org/10.1111/gcb.15161 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    46.
    Tarran, G. A., Heywood, J. L. & Zubkov, M. V. Latitudinal changes in the standing stocks of nano- and picoeukaryotic phytoplankton in the Atlantic Ocean. Deep Res. Part II Top. Stud. Oceanogr. 53, 1516–1529 (2006).
    ADS  Article  Google Scholar 

    47.
    Marañón, E., Cermeño, P., Latasa, M. & Tadonléké, R. D. Temperature, resources, and phytoplankton size structure in the ocean. Limnol. Oceanogr. 57, 1266–1278 (2012).
    ADS  Article  Google Scholar 

    48.
    Chisholm, S. W. Phytoplankton Size. Prim. Product. Biogeochem. Cycles Sea 02139, 213–237 (1992).
    Article  Google Scholar 

    49.
    Montes-Pérez, J. J. et al. Intermediate-size cell dominance in the phytoplankton community of an eutrophic, estuarine ecosystem (Guadalhorce River, Southern Spain). Hydrobiologia 847, 2241–2254 (2020).
    Article  CAS  Google Scholar 

    50.
    Chen, B. & Laws, E. A. Is there a difference of temperature sensitivity between marine phytoplankton and heterotrophs?. Limnol. Oceanogr. 62, 806–817 (2016).
    ADS  Article  Google Scholar 

    51.
    Eppley, R. W. Temperature and phytoplankton growth in the sea. Fish. Bull. 70, 1063–1085 (1972).
    Google Scholar 

    52.
    Johnson, F. & Lewin, I. The growth rate of E. coli in relation to temperature, Quinine and Coenzyme. J. Cell Physiol. 28, 47–75 (1946).
    CAS  Article  Google Scholar 

    53.
    Dell, A. I., Pawar, S. & Savage, V. M. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl. Acad. Sci. U.S.A. 108, 10591–10596 (2011).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar  More

  • in

    Separate and combined Hanseniaspora uvarum and Metschnikowia pulcherrima metabolic volatiles are attractive to Drosophila suzukii in the laboratory and field

    1.
    Bolda, M. P., Goodhue, R. E. & Zalom, F. G. Spotted wing drosophila: Potential economic impact of a newly established pest. Agric. Resour. Econ. Update 13, 5–8 (2010).
    Google Scholar 
    2.
    Calabria, G., Máca, J., Bächli, G., Serra, L. & Pascual, M. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J. Appl. Entomol. 136, 139–147 (2012).
    Article  Google Scholar 

    3.
    Harris, A. & Shaw, B. First record of Drosophila suzukii (Matsumura) (Diptera, Drosophilidae) in Great Britain. Dipterists Digest. 21, 189–192 (2014).
    Google Scholar 

    4.
    Atallah, J., Teixeira, L., Salazar, R., Zaragoza, G. & Kopp, A. The making of a pest: The evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proc. R. Soc. B Biol. Sci. 281, 20132840. https://doi.org/10.1098/rspb.2013.2840 (2014).
    Article  Google Scholar 

    5.
    Rombaut, A. et al. Invasive Drosophila suzukii facilitates Drosophila melanogaster infestation and sour rot outbreaks in the vineyards. R. Soc. Open Sci. 4, 170117. https://doi.org/10.1098/rsos.170117 (2017).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    6.
    Gress, B. E. & Zalom, F. G. Identification and risk assessment of spinosad resistance in a California population of Drosophila suzukii. Pest Manag. Sci. 75, 1270–1276. https://doi.org/10.1002/ps.5240 (2019).
    CAS  Article  PubMed  Google Scholar 

    7.
    Lee, K. P. et al. Lifespan and reproduction in Drosophila: New insights from nutritional geometry. Proc. Natl. Acad. Sci. 105, 2498–2503 (2008).
    ADS  CAS  Article  Google Scholar 

    8.
    Piper, M. D. W. et al. A holidic medium for Drosophila melanogaster. Nat. Methods 11, 100–105. https://doi.org/10.1038/nmeth.2731 (2014).
    CAS  Article  PubMed  Google Scholar 

    9.
    Grangeteau, C. et al. Yeast quality in juvenile diet affects Drosophila melanogaster adult life traits. Sci. Rep. 8, 13070. https://doi.org/10.1038/s41598-018-31561-9 (2018).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    10.
    Rohlfs, M. & Kürschner, L. Saprophagous insect larvae, Drosophila melanogaster, profit from increased species richness in beneficial microbes. J. Appl. Entomol. 134, 667–671. https://doi.org/10.1111/j.1439-0418.2009.01458.x (2009).
    Article  Google Scholar 

    11.
    Hardin, J. A., Kraus, D. A. & Burrack, H. J. Diet quality mitigates intraspecific larval competition in Drosophila suzukii. Entomol. Exp. Appl. 156, 59–65. https://doi.org/10.1111/eea.12311 (2015).
    CAS  Article  Google Scholar 

    12.
    Lewis, M. T. & Hamby, K. A. Differential impacts of yeasts on feeding behavior and development in larval Drosophila suzukii (Diptera:Drosophilidae). Sci. Rep. 9, 13370. https://doi.org/10.1038/s41598-019-48863-1 (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    13.
    Bellutti, N. et al. Dietary yeast affects preference and performance in Drosophila suzukii. J. Pest. Sci. 91, 651–660 (2018).
    Article  Google Scholar 

    14.
    Buser, C. C., Newcomb, R. D., Gaskett, A. C. & Goddard, M. R. Niche construction initiates the evolution of mutualistic interactions. Ecol. Lett. 17, 1257–1264. https://doi.org/10.1111/ele.12331 (2014).
    Article  PubMed  Google Scholar 

    15.
    Günther, C. S., Knight, S. J., Jones, R. & Goddard, M. R. Are Drosophila preferences for yeasts stable or contextual?. Ecol. Evol. 9, 8075–8086. https://doi.org/10.1002/ece3.5366 (2019).
    Article  PubMed  PubMed Central  Google Scholar 

    16.
    Christiaens, J. F. et al. The fungal aroma gene ATF1 promotes dispersal of yeast cells through insect vectors. Cell Rep. 9, 425–432. https://doi.org/10.1016/j.celrep.2014.09.009 (2014).
    CAS  Article  PubMed  Google Scholar 

    17.
    Palanca, L., Gaskett, A. C., Günther, C. S., Newcomb, R. D. & Goddard, M. R. Quantifying variation in the ability of yeasts to attract Drosophila melanogaster. PLoS ONE 8, e75332. https://doi.org/10.1371/journal.pone.0075332 (2013).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    18.
    Scheidler, N. H., Liu, C., Hamby, K. A., Zalom, F. G. & Syed, Z. Volatile codes: Correlation of olfactory signals and reception in Drosophila-yeast chemical communication. Sci. Rep. 5, 1–13. https://doi.org/10.1038/srep14059 (2015).
    CAS  Article  Google Scholar 

    19.
    Becher, P. G. et al. Chemical signaling and insect attraction is a conserved trait in yeasts. Ecol. Evol. 8, 2962–2974. https://doi.org/10.1002/ece3.3905 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    20.
    Chandler, J. A., Eisen, J. A. & Kopp, A. Yeast communities of diverse Drosophila species: Comparison of two symbiont groups in the same hosts. Appl. Environ. Microbiol. 78, 7327–7336. https://doi.org/10.1128/AEM.01741-12 (2012).
    CAS  Article  PubMed  Google Scholar 

    21.
    Lam, S. S. T. H. & Howell, K. S. Drosophila-associated yeast species in vineyard ecosystems. FEMS Microbiol. Lett. 362, 1–7. https://doi.org/10.1093/femsle/fnv170 (2015).
    CAS  Article  Google Scholar 

    22.
    Hamby, K. A., Hernández, A., Boundy-Mills, K. & Zalom, F. G. Associations of yeasts with spotted-wing Drosophila (Drosophila suzukii; Diptera: Drosophilidae) in cherries and raspberries. Appl. Environ. Microbiol. 78, 4869–4873. https://doi.org/10.1128/AEM.00841-12 (2012).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    23.
    Lewis, M. T., Koivunen, E. E., Swett, C. L. & Hamby, K. A. Associations between Drosophila suzukii (Diptera: Drosophilidae) and fungi in raspberries. Environ. Entomol. 27, 383–392. https://doi.org/10.1093/ee/nvy167 (2018).
    Article  Google Scholar 

    24.
    Fountain, M. T. et al. Alimentary microbes of winter-form Drosophila suzukii. Insect Mol. Biol. 27, 383–392. https://doi.org/10.1111/imb.12377 (2018).
    CAS  Article  PubMed  Google Scholar 

    25.
    Vadkertiová, R., Molnárová, J., Vránová, D. & Sláviková, E. Yeasts and yeast-like organisms associated with fruits and blossoms of different fruit trees. Can. J. Microbiol. 58, 1344–1352. https://doi.org/10.1139/cjm-2012-0468 (2012).
    CAS  Article  PubMed  Google Scholar 

    26.
    Barata, A., Malfeito-Ferreira, M. & Loureiro, V. Changes in sour rotten grape berry microbiota during ripening and wine fermentation. Int. J. Food Microbiol. 154, 152–161. https://doi.org/10.1016/J.IJFOODMICRO.2011.12.029 (2012).
    CAS  Article  PubMed  Google Scholar 

    27.
    Lasa, R. et al. Yeast species, strains, and growth media mediate attraction of Drosophila suzukii (Diptera: Drosophilidae). Insects 10, 228–228. https://doi.org/10.3390/insects10080228 (2019).
    Article  PubMed Central  Google Scholar 

    28.
    Noble, R. et al. Improved insecticidal control of spotted wing drosophila (Drosophila suzukii) using yeast and fermented strawberry juice baits. Crop Protect. https://doi.org/10.1016/J.CROPRO.2019.104902 (2019).
    Article  Google Scholar 

    29.
    Hoang, D., Kopp, A. & Chandler, J. A. Interactions between Drosophila and its natural yeast symbionts—Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?. PeerJ 3, e1116. https://doi.org/10.7717/peerj.1116 (2015).
    Article  PubMed  PubMed Central  Google Scholar 

    30.
    Taylor, M. W., Tsai, P., Anfang, N., Ross, H. A. & Goddard, M. R. Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environ. Microbiol. 16, 2848–2858. https://doi.org/10.1111/1462-2920.12456 (2014).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    31.
    Abdelfattah, A., Wisniewski, M., Li Destri Nicosia, M. G., Cacciola, S. O. & Schena, L. Metagenomic analysis of fungal diversity on strawberry plants and the effect of management practices on the fungal community structure of aerial organs. PLoS ONE 11, e0160470. https://doi.org/10.1371/journal.pone.0160470 (2016).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    32.
    Dobzhansky, T., Cooper, D. M., Phaff, H. J., Knapp, E. P. & Carson, H. L. Differential attraction of species of Drosophila to different species of yeasts. Ecology 37, 544–550. https://doi.org/10.2307/1930178 (1956).
    Article  Google Scholar 

    33.
    Günther, C. S. & Goddard, M. R. Do yeasts and Drosophila interact just by chance?. Fungal Ecol. 38, 37–43. https://doi.org/10.1016/J.FUNECO.2018.04.005 (2018).
    Article  Google Scholar 

    34.
    Günther, C. S., Goddard, M. R., Newcomb, R. D. & Buser, C. C. The context of chemical communication driving a mutualism. J. Chem. Ecol. 41, 929–936. https://doi.org/10.1007/s10886-015-0629-z (2015).
    CAS  Article  PubMed  Google Scholar 

    35.
    Schiabor, K. M., Quan, A. S. & Eisen, M. B. Saccharomyces cerevisiae mitochondria are required for optimal attractiveness to Drosophila melanogaster. PLoS ONE 9, e113899. https://doi.org/10.1371/journal.pone.0113899 (2014).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

    36.
    Gayevskiy, V. & Goddard, M. R. Geographic delineations of yeast communities and populations associated with vines and wines in New Zealand. ISME J. 6, 1281–1290 (2012).
    CAS  Article  Google Scholar 

    37.
    Bokulich, N. A., Thorngate, J. H., Richardson, P. M. & Mills, D. A. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc. Natl. Acad. Sci. 111, E139–E148. https://doi.org/10.1073/PNAS.1317377110 (2014).
    ADS  CAS  Article  PubMed  Google Scholar 

    38.
    Martins, G. et al. Influence of the farming system on the epiphytic yeasts and yeast-like fungi colonizing grape berries during the ripening process. Int. J. Food Microbiol. 177, 21–28. https://doi.org/10.1016/J.IJFOODMICRO.2014.02.002 (2014).
    Article  PubMed  Google Scholar 

    39.
    Cordero-Bueso, G. et al. Influence of the farming system and vine variety on yeast communities associated with grape berries. Int. J. Food Microbiol. 145, 132–139. https://doi.org/10.1016/J.IJFOODMICRO.2010.11.040 (2011).
    Article  PubMed  Google Scholar 

    40.
    Cha, D. H., Adams, T., Rogg, H. & Landolt, P. J. Identification and field evaluation of fermentation volatiles from wine and vinegar that mediate attraction of spotted wing drosophila, Drosophila suzukii. J. Chem. Ecol. 38, 1419–1431. https://doi.org/10.1007/s10886-012-0196-5 (2012).
    CAS  Article  PubMed  Google Scholar 

    41.
    Cha, D. H. et al. A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Manag. Sci. 70, 324–331. https://doi.org/10.1002/ps.3568 (2014).
    CAS  Article  PubMed  Google Scholar 

    42.
    Faucher, C. P., Hilker, M. & de Bruyne, M. Interactions of carbon dioxide and food odours in Drosophila: Olfactory hedonics and sensory neuron properties. PLoS ONE 8, e56361 (2013).
    ADS  CAS  Article  Google Scholar 

    43.
    Liti, G. et al. Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009).
    ADS  CAS  Article  Google Scholar 

    44.
    Knight, S., Klaere, S., Fedrizzi, B. & Goddard, M. R. Regional microbial signatures positively correlate with differential wine phenotypes: Evidence for a microbial aspect to terroir. Sci. Rep. 5, 1–10. https://doi.org/10.1038/srep14233 (2015).
    CAS  Article  Google Scholar 

    45.
    Albertin, W. et al. Hanseniaspora uvarum from winemaking environments show spatial and temporal genetic clustering. Front. Microbiol. 6, 1569 (2016).
    Article  Google Scholar 

    46.
    Shearer, P. W. et al. Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecol. 16, 11. https://doi.org/10.1186/s12898-016-0070-3 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    47.
    Tochen, S. et al. Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ. Entomol. 43, 501–510. https://doi.org/10.1603/EN13200 (2014).
    Article  PubMed  Google Scholar 

    48.
    Ryan, G. D., Emiljanowicz, L., Wilkinson, F., Kornya, M. & Newman, J. A. Thermal tolerances of the spotted-wing drosophila Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol 109, 746–752. https://doi.org/10.1093/jee/tow006 (2016).
    Article  PubMed  Google Scholar 

    49.
    Plantamp, C., Estragnat, V., Fellous, S., Desouhant, E. & Gibert, P. Where and what to feed? Differential effects on fecundity and longevity in the invasive Drosophila suzukii. Basic Appl. Ecol. 19, 56–66. https://doi.org/10.1016/j.baae.2016.10.005 (2017).
    Article  Google Scholar 

    50.
    Anfang, N., Brajkovich, M. & Goddard, M. R. Co-fermentation with Pichia kluyveri increases varietal thiol concentrations in Sauvignon Blanc. Aust. J. Grape Wine Res. 15, 1–8 (2009).
    CAS  Article  Google Scholar 

    51.
    Fischer, C. et al. Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior. eLife 6, e18855. https://doi.org/10.7554/eLife.18855 (2017).
    Article  PubMed  PubMed Central  Google Scholar 

    52.
    Mori, B. A. et al. Enhanced yeast feeding following mating facilitates control of the invasive fruit pest Drosophila suzukii. J. Appl. Ecol. 54, 170–177. https://doi.org/10.1111/1365-2664.12688 (2017).
    Article  Google Scholar 

    53.
    Shaw, B., Brain, P., Wijnen, H. & Fountain, M. T. Reducing Drosophila suzukii emergence through inter-species competition. Pest Manag. Sci. 74, 149–160. https://doi.org/10.1002/ps.4836 (2018).
    CAS  Article  Google Scholar 

    54.
    Cini, A., Ioriatti, C. & Anfora, G. A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull. Insectol. 65, 149–160 (2012).
    Google Scholar 

    55.
    Crawley, M. J. The R book (Wiley, New York, 2013).
    Google Scholar 

    56.
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2019).
    Google Scholar 

    57.
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
    Article  Google Scholar 

    58.
    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Estimated marginal means, aka least-squares means. R package version 1.3. 2. (2019).

    59.
    Harrell, F. E., et al. Hmisc: Harrell Miscellaneous. R package version 4.3–1. (2020). More

  • in

    Temporal division of labor in an aphid social system

    1.
    Wilson, E. O. The Insect Societies (Harvard University Press, Cambridge, 1971).
    Google Scholar 
    2.
    Wilson, E. O. Sociobiology: The New Synthesis (Harvard University Press, Cambridge, 1975).
    Google Scholar 

    3.
    Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects (Princeton University Press, Princeton, 1978).
    Google Scholar 

    4.
    Seeley, T. D. Honeybee Ecology: A Study of Adaptation in Social Life (Princeton University Press, Princeton, 1985).
    Google Scholar 

    5.
    Seeley, T. D. Adaptive significance of the age polyethism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 11, 287–293 (1982).
    Article  Google Scholar 

    6.
    Robinson, G. E. Regulation of division of labor in insect societies. Annu. Rev. Entomol. 37, 637–665 (1992).
    CAS  PubMed  Article  Google Scholar 

    7.
    Beshers, S. N. & Fewell, J. H. Models of division of labor in social insects. Annu. Rev. Entomol. 46, 413–440 (2001).
    CAS  PubMed  Article  Google Scholar 

    8.
    Johnson, B. R. Within-nest temporal polyethism in the honey bee. Behav. Ecol. Sociobiol. 62, 777–784 (2008).
    Article  Google Scholar 

    9.
    Hölldobler, B. & Wilson, E. O. The Ants (Harvard University Press, Cambridge, 1990).
    Google Scholar 

    10.
    Crosland, M. W. J., Lok, C. M., Wong, T. C., Shakarad, M. & Traniello, J. F. A. Division of labour in a lower termite: The majority of tasks are performed by older workers. Anim. Behav. 54, 999–1012 (1997).
    CAS  PubMed  Article  Google Scholar 

    11.
    Hinze, B. & Leuthold, R. H. Age related polyethism and activity rhythms in the nest of the termite Macrotermes bellicosus (Isoptera, Termitidae). Insect. Soc. 46, 392–397 (1999).
    Article  Google Scholar 

    12.
    Cameron, S. A. Temporal patterns of division of labor among workers in the primitively eusocial bumble bee, Bombus griseocoffis (Hymenoptera: Apidae). Ethology 80, 137–151 (1989).
    Article  Google Scholar 

    13.
    Naug, D. & Gadagkar, R. The role of age in temporal polyethism in a primitively eusocial wasp. Behav. Ecol. Sociobiol. 42, 37–47 (1998).
    Article  Google Scholar 

    14.
    Biedermann, P. H. W. & Taborsky, M. Larval helpers and age polyethism in ambrosia beetles. Proc. Natl. Acad. Sci. USA 108, 17064–17069 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    15.
    Wakano, J. N., Nakata, K. & Yamamura, N. Dynamic model of optimal age polyethism in social insects under stable and fluctuating environments. J. Theor. Biol. 193, 153–165 (1998).
    Article  Google Scholar 

    16.
    Duarte, A., Weissing, F. J., Pen, I. & Keller, L. An evolutionary perspective on self-organized division of labor in social insects. Annu. Rev. Ecol. Evol. Syst. 42, 91–110 (2011).
    Article  Google Scholar 

    17.
    Stern, D. L. & Foster, W. A. The evolution of soldiers in aphids. Biol. Rev. 71, 27–79 (1996).
    CAS  PubMed  Article  Google Scholar 

    18.
    Aoki, S. & Kurosu, U. A review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche 2010, 380351 (2010).
    Google Scholar 

    19.
    Abbot, P., Tooker, J. & Lawson, S. P. Chemical ecology and sociality in aphids: Opportunities and directions. J. Chem. Ecol. 44, 770–784 (2018).
    CAS  PubMed  Article  Google Scholar 

    20.
    Aoki, S. Colophina clematis (Homoptera, Pemphigidae), an aphid species with” soldiers”. Kontyu 5, 276–282 (1977).
    Google Scholar 

    21.
    Aoki, S. & Kurosu, U. Gall cleaning by the aphid Hormaphis betulae. J. Ethol. 9, 51–55 (1989).
    Google Scholar 

    22.
    Benton, T. G. & Foster, W. A. Altruistic housekeeping in a social aphid. Proc. R. Soc. B 247, 199–202 (1992).
    ADS  Article  Google Scholar 

    23.
    Aoki, S. & Kurosu, U. Soldiers of Astegopteryx styraci (Homoptera, Aphidoidea) clean their gall. Jpn. J. Entomol. 57, 407–416 (1989).
    Google Scholar 

    24.
    Aoki, S., Kurosu, U. & Stern, D. L. Aphid soldiers discriminate between soldiers and non-soldiers, rather than between kin and non-kin Ceratoglyphina bambusae. Anim. Behav. 42, 865–866 (1991).
    Article  Google Scholar 

    25.
    Kurosu, U., Narukawa, J., Buranapanichpan, S. & Aoki, S. Head-plug defense in a gall aphid. Insect. Soc. 53, 86–91 (2006).
    Article  Google Scholar 

    26.
    Kurosu, U., Aoki, S. & Fukatsu, T. Self-sacrificing gall repair by aphid nymphs. Proc. R. Soc. B 270, S12–S14 (2003).
    PubMed  Article  Google Scholar 

    27.
    Pike, N. & Foster, W. Fortress repair in the social aphid species Pemphigus spyrothecae. Anim. Behav. 67, 909–914 (2004).
    Article  Google Scholar 

    28.
    Kutsukake, M., Shibao, H., Uematsu, K. & Fukatsu, T. Scab formation and wound healing of plant tissue by soldier aphid. Proc. R. Soc. B 276, 1555–1563 (2009).
    PubMed  Article  Google Scholar 

    29.
    Kutsukake, M. et al. Exaggeration and cooption of innate immunity for social defense. Proc. Natl. Acad. Sci. USA 116, 8950–8959 (2019).
    CAS  PubMed  Article  Google Scholar 

    30.
    Aoki, S. Evolution of sterile soldiers in aphids. In Animal Societies: Theories andFacts (eds Ito, Y. et al.) 53–65 (Japan Scientific Societies Press, Tokyo, 1987).
    Google Scholar 

    31.
    Aoki, S. & Kurosu, U. Social aphids. In Encyclopedia of Social Insects (ed. Starr, C. K.) (Springer, New York, 2020). https://doi.org/10.1007/978-3-319-90306-4_107-1.
    Google Scholar 

    32.
    Aoki, S. & Kurosu, U. Biennial galls of the aphid Astegopteryx styraci on a temperate deciduous tree Styrax obassia. Acta Phytopathol. Entomol. Hung. 25, 57–65 (1990).
    Google Scholar 

    33.
    Shibao, H., Kutsukake, M., Lee, J. & Fukatsu, T. Maintenance of soldier-producing aphids on an artificial diet. J. Insect Physiol. 48, 495–505 (2002).
    CAS  PubMed  Article  Google Scholar 

    34.
    Shibao, H., Lee, J. M., Kutsukake, M. & Fukatsu, T. Aphid soldier differentiation: density acts on both embryos and newborn nymphs. Naturwissenschaften 90, 501–504 (2003).
    ADS  CAS  PubMed  Article  Google Scholar 

    35.
    Shibao, H., Kutsukake, M. & Fukatsu, T. Density triggers soldier production in a social aphid. Proc. R. Soc. B 271, S71–S74 (2004).
    PubMed  Article  Google Scholar 

    36.
    Shibao, H., Kutsukake, M. & Fukatsu, T. The proximate cue of density-dependent soldier production in a social aphid. J. Insect Physiol. 50, 143–147 (2004).
    CAS  PubMed  Article  Google Scholar 

    37.
    Shibao, H., Kutsukake, M. & Fukatsu, T. Density-dependent induction and suppression of soldier differentiation in an aphid social system. J. Insect Physiol. 50, 995–1000 (2004).
    CAS  PubMed  Article  Google Scholar 

    38.
    Shibao, H., Kutsukake, M., Matsuyama, S., Fukatsu, T. & Shimada, M. Mechanisms regulating caste differentiation in an aphid social system. Commun. Integr. Biol. 3, 1–5 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    39.
    Kutsukake, M. et al. Venomous protease of aphid soldier for colony defense. Proc. Natl. Acad. Sci. USA 101, 11338–11343 (2004).
    ADS  CAS  PubMed  Article  Google Scholar 

    40.
    Stern, D. L., Aoki, S. & Kurosu, U. A test of geometric hypotheses for soldier investment patterns in the gall producing tropical aphid Cerataphis fransseni (Homoptera, Hormaphididae). Insect. Soc. 41, 457–460 (1994).
    Article  Google Scholar 

    41.
    Pike, N., Braendle, C. & Foster, W. A. Seasonal extension of the soldier instar as a route to increased defence investment in the social aphid Pemphigus spyrothecae. Ecol. Entomol. 29, 89–95 (2004).
    Article  Google Scholar 

    42.
    Pike, N. Specialised placement of morphs within the gall of the social aphid Pemphigus spyrothecae. BMC Evol. Biol. 7, 18 (2007).
    PubMed  PubMed Central  Article  Google Scholar 

    43.
    Uematsu, K., Kutsukake, M., Fukatsu, T., Shimada, M. & Shibao, H. Altruistic colony defense by menopausal female insects. Curr. Biol. 20, 1182–1186 (2010).
    CAS  PubMed  Article  Google Scholar 

    44.
    Uematsu, K., Shimada, M. & Shibao, H. Juveniles and the elderly defend, the middle-aged escape: division of labour in a social aphid. Biol. Let. 9, 20121053 (2013).
    Article  Google Scholar 

    45.
    Abe, T., Bignell, D. E., Higashi, M. & Abe, Y. Termites: Evolution, Sociality, Symbioses, Ecology (Springer, Berlin, 2000).
    Google Scholar 

    46.
    Shibao, H. Lack of kin discrimination in the eusocial aphid Pseudoregma bambucicola (Homoptera: Aphididae). J. Ethol. 17, 17–24 (1999).
    Article  Google Scholar 

    47.
    Abbot, P., Withgott, J. H. & Moran, N. A. Genetic conflict and conditional altruism in social aphid colonies. Proc. Natl. Acad. Sci. USA 98, 12068–12071 (2001).
    ADS  CAS  PubMed  Article  Google Scholar 

    48.
    Abbot, P. & Chhatre, V. Kin structure provides no explanation for intruders in social aphids. Mol. Ecol. 16, 3659–3670 (2007).
    CAS  PubMed  Article  Google Scholar 

    49.
    Kutsukake, M. et al. An insect-induced novel plant phenotype for sustaining social life in a closed system. Nat. Commun. 3, 1187 (2012).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    50.
    Kutsukake, M. et al. Evolution of soldier-specific venomous protease in social aphids. Mol. Biol. Evol. 25, 2627–2641 (2008).
    CAS  PubMed  Article  Google Scholar  More

  • in

    Decreased cortisol among hikers who preferentially visit and value biodiverse riparian zones

    Study areas
    We collected survey and salivary hormone data from people at the Camel’s Back—Hulls Gulch Reserve of the Ridge to Rivers Management Area in Boise, Idaho, USA (Fig. 1S). The Lower Hulls Gulch area is largely characterized by sagebrush steppe habitat as well as riparian areas that act as habitat to a variety of avian, mammal, and herpetological species. Common wildlife spotted by recreationists include birds, amphibians, reptiles, and small mammals. We collected data between March 24—May 18, 2017 on both the weekend and weekdays. Weather data, consisting of average wind speed and average air temperature were taken from the Crestline Trail Idaho (Boise, ID).
    Participants
    We recruited participants at a prominent trail head associated with the recreational area, and the purpose and protocols of the study were explained. Upon agreeing to participate, participants were asked to read an additional written statement of the project and sign a informed consent form. Each recruited individual was minimally required to participate in either the saliva collection or survey, although participation in all parts of the study was highly encouraged. Any recreationists who had been recreating for more than 10 min were not recruited. We defined hikers as recreationists who were intent on walking in the recreational area, and excluded users who were performing exertive activities such as running or biking. All participants were given an anonymous identifier which was used throughout the study. This research project was reviewed and approved by the IRB at Boise State University, Idaho, USA under #006-SB17-061.
    Salivary cortisol and testosterone collection
    We restricted all sampling until late morning (often 10:00am) to control for diel patterns in hormone concentrations after awakening25,26,27. To further account for any variations due to time of day, the time of collection was recorded for each saliva sample and factored into each analysis. We found that the time of day each cortisol sample was taken did not account for variation, and that the diurnal cycle of cortisol did not explain the change in cortisol concentration that we observed in hikers.
    Saliva samples were collected from recreationists using a pre-post paired design. Participants were asked to give at least 0.25 mL of saliva using a saliva collection aid (2 mL cyrovial, Salimetrics PA, USA) via the passive drool method25,28. The passive drool method allows for the collection of large samples for multiple assays, reduces the risk of contamination by collection substances, and allows samples to be frozen without interfering with assay protocols28. Saliva was immediately stored in a portable cooler with ice until frozen at -10 °C. Cortisol and testosterone concentrations were assessed using a Salimetrics Cortisol Enzyme Immunoassay following the manufacturer’s protocols and design (Salimetrics, PA, USA). All assay plates were read using the Gen5 software and Biotek EL800 Plate Reader. Hormone concentrations were then calculated from the optical densities using a standard curve and the online elisaanalysis interface.
    Survey collection
    After recreating, all participants were asked to take a survey. Survey questions included the following: variables affecting psychological stress levels, observation of wildlife, motivations for recreation (ranging from social, personal challenge, wildlife, and solitude), perceived ecological impact that outdoor recreational activity has on wildlife and habitats, and basic demographics including age and gender. In addition, participants were asked to rate how psychologically stressed they felt after their recreational activity. Participants also had the opportunity to note any negative experiences they had while recreating.
    GPS track collection
    Participants were encouraged to carry a handheld GPS device to track their route while hiking. We used GPS tracks to connect hiker routes with land cover types such as % vegetation cover, urban cover, water, and riparian cover. Using a 100 m buffer as a standard measurement for visibility, we calculated the proportion of land cover types each hiker traveled through during their trip. We also used GPS tracks to compare line density calculations to estimate areas and trails with higher recreational traffic.
    Photograph collection
    We used volunteer employed photography and asked participants to take photographs of landscapes they found beautiful. At the end of the trip, participants were asked to select one photograph that captured an area of high aesthetic value to them. Photographs were spatially linked to the landscape using participant GPS tracks, and analyzed using kernel density estimates (KDE) to compare what areas and land cover types were photographed more frequently. In addition, the subject and photographic elements of each photograph were tallied and collected to compare what components of the landscape participants were more likely to take pictures of.
    Statistical analyses
    To assess the change in salivary cortisol to landscape aesthetics, we used a backward stepwise approach to create a linear model with the following predictor variables: perceived aesthetics (using principal component PC1 scores), land cover metrics, start time, duration, total wildlife observance, plant identification skills (as a measure of ecological familiarity), and all aesthetic interaction terms. . We checked for collinearity among variables and considered pairwise r  >|0.70| to indicate a correlation. Due to high correlation between start time and duration, duration was removed from all models. A total of 6 saliva samples (all hikers) were not used due to unusually high ( > 2 SD) cortisol concentrations.
    Non-significant interaction variables were removed first based on lowest SS values, followed by main effect variables with the lowest SS value until only statistically significant variables remained. Cortisol was evaluated as the change in concentration from recreational activity (Post-collection—Pre-collection). Negative changes correspond to a decrease and positive changes to an increase in hormone concentration after recreating. To meet normality assumptions, the change in both cortisol was transformed using a square root function taken at absolute value. After data transformation, all original signs were returned to maintain the negative–positive spectrum of hormone change. The removal of any outliers did not change the interpretation of the results and were kept across analyses.
    We used a backward stepwise approach to explain aesthetic perception with the following predictor variables: weekend/weekday (as a metric of visitor use), total wildlife observance, plant identification skills (as a metric of ecological familiarity), gender, age, duration, and all interaction terms. We used a backward stepwise approach and a generalized linear model to evaluate whether land cover, recreational use, and ecological familiarity explained the number of wildlife observations.No variables were correlated with each other, and all interaction terms were included. To investigate the relationship between perceived ecological impact metrics and recreational motivation, we used spearman correlations. More

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    Water constraints drive allometric patterns in the body shape of tree frogs

    1.
    Adams, D. C. & Nistri, A. Ontogenetic convergence and evolution of foot morphology in european cave salamanders (Family: Plethodontidae). BMC Evol. Biol. 10, 216 (2010).
    PubMed  PubMed Central  Article  Google Scholar 
    2.
    Baken, E. K., Mellenthin, L. E. & Adams, D. C. Macroevolution of desiccation-related morphology in plethodontid salamanders as inferred from a novel surface area to volume ratio estimation approach. Evolution 74, 476–486 (2020).
    PubMed  Article  Google Scholar 

    3.
    Martinez, P. A. et al. The contribution of neutral evolution and adaptive processes in driving phenotypic divergence in a model mammalian species, the andean fox Lycalopex culpaeus. J. Biogeogr. 45, 1114–1125 (2018).
    Article  Google Scholar 

    4.
    Vidal-García, M., Byrne, P. G., Roberts, J. D. & Keogh, J. S. The role of phylogeny and ecology in shaping morphology in 21 genera and 127 species of australo-papuan myobatrachid frogs. J. Evol. Biol. 27, 181–192 (2014).
    PubMed  Article  Google Scholar 

    5.
    Adams, D. C. Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evol. Biol. 10, 72 (2010).
    PubMed  PubMed Central  Article  Google Scholar 

    6.
    Losos, J. B. Ecological character displacement and the study of adaptation. Proc. Natl. Acad. Sci. 97, 5693–5695 (2000).
    ADS  CAS  PubMed  Article  Google Scholar 

    7.
    Moen, D. S., Irschick, D. J. & Wiens, J. J. Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proc. R. Soc. B. 280, 20132156 (2013).
    PubMed  Article  Google Scholar 

    8.
    Amado, T. F., Bidau, C. J. & Olalla-Tárraga, M. Á. Geographic variation of body size in new world anurans: energy and water in a balance. Ecography 42, 456–466 (2019).
    Article  Google Scholar 

    9.
    Gouveia, S. F. et al. Biophysical modeling of water economy can explain geographic gradient of body size in anurans. Am. Nat. 193, 51–58 (2019).
    PubMed  Article  PubMed Central  Google Scholar 

    10.
    Olalla-Tárraga, M. Á., Diniz-Filho, J. A. F., Bastos, R. P. & Rodríguez, M. Á. Geographic body size gradients in tropical regions: water deficit and anuran body size in the brazilian cerrado. Ecography 32, 581–590 (2009).
    Article  Google Scholar 

    11.
    Cooney, C. R. et al. Ecology and allometry predict the evolution of avian developmental durations. Nat. Commun. 11, 1–9 (2020).
    Article  CAS  Google Scholar 

    12.
    Kriegman, S., Cheney, N. & Bongard, J. How morphological development can guide evolution. Sci. Rep. 8, 1–10 (2018).
    Article  CAS  Google Scholar 

    13.
    Moczek, A. P. Re-evaluating the environment in developmental evolution. Front. Ecol. Evol. 3, 1–8 (2015).
    Article  Google Scholar 

    14.
    Richter-Boix, A., Tejedo, M. & Rezende, E. L. Evolution and plasticity of anuran larval development in response to desiccation. a comparative analysis. Ecol. Evol. 1, 15–25 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    15.
    Castro, K. M. S. A., do Santos, M. P., Brito, M. F. G., Bidau, C. J. & Martinez, P. A. Ontogenetic allometry conservatism across five teleost orders. J. Fish Biol. 93, 745–749 (2018).
    Article  Google Scholar 

    16.
    Skúlason, S. et al. A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems. Biol. Rev. 94, 1786–1808 (2019).
    PubMed  Article  Google Scholar 

    17.
    Porter, W. P. & Gates, D. M. Thermodynamic equilibria of animals with environment. Ecol. Monogr. 39, 227–244 (1969).
    Article  Google Scholar 

    18.
    Thompson, D. A. On Growth and Form (Cambridge University Press, Cambridge, 1917).
    Google Scholar 

    19.
    Schmidt-Nielsen, K. Scaling: Why is Animal Size so Important? (Cambridge University Press, Cambridge, 1984).
    Google Scholar 

    20.
    Amado, T. F., Pinto, M. G. M. & Olalla-Tárraga, M. Á. Anuran 3d models reveal the relationship between surface area-to-volume ratio and climate. J. Biogeogr. 46, 1429–1437 (2019).
    Google Scholar 

    21.
    Ashton, K. G. Do amphibians follow bergmann’s rule?. Can. J. Zool. 80, 708–716 (2002).
    Article  Google Scholar 

    22.
    Glazier, D. Effects of contingency versus constraints on the body-mass scaling of metabolic rate. Challenges 9, 4 (2018).
    Article  Google Scholar 

    23.
    Gouveia, S. F. & Correia, I. Geographical clines of body size in terrestrial amphibians: water conservation hypothesis revisited. J. Biogeogr. 43, 2075–2084 (2016).
    Article  Google Scholar 

    24.
    Lindsey, C. C. Body sizes of poikilotherm vertebrates at different latitudes. Evolution 20, 456–465 (1966).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    25.
    Bergmannn, C. Über die verhältnisse der wärmeökonomie der thiere zu ihrer grösse. Göttinger Stud. 1, 595–708 (1847).
    Google Scholar 

    26.
    Nevo, E. Adaptive variation in size of cricket frogs. Ecology 54, 1271–1281 (1973).
    Article  Google Scholar 

    27.
    Tracy, C. R., Christian, K. A. & Tracy, C. R. Not just small, wet, and cold : effects of body size and skin resistance on thermoregulation and arboreality of frogs. Ecology 91, 1477–1484 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    28.
    Wells, K. D. The Ecology and Behavior of Amphibians (The University of Chicago Press, Chicago, 2007).
    Google Scholar 

    29.
    Perez, D., Sheehy, C. M. & Lillywhite, H. B. Variation of organ position in snakes. J. Morphol. 280, 1798–1807 (2019).
    PubMed  Article  PubMed Central  Google Scholar 

    30.
    Amiel, J. J., Chua, B., Wassersug, R. J. & Jones, D. R. Temperature-dependent regulation of blood distribution in snakes. J. Exp. Biol. 214, 1458–1462 (2011).
    PubMed  Article  PubMed Central  Google Scholar 

    31.
    Canals, M. Thermal ecology of small animals. Biol Res 31, 367–374 (1998).
    Google Scholar 

    32.
    Tracy, C. R. A model of the dynamic exchanges of water and energy between a terrestrial amphibian and its environment. Ecol. Monogr. 46, 293–326 (1976).
    Article  Google Scholar 

    33.
    Gould, S. J. Allometry and size in ontogeny and phylogeny. Biol. Rev. 41, 587–640 (1966).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    34.
    Klingenberg, C. P. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol. Rev. 73, 79–123 (1998).
    CAS  PubMed  Article  Google Scholar 

    35.
    Klingenberg, C. P. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev. Genes Evol. 226, 113–137 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    36.
    Voje, K. L., Hansen, T. F., Egset, C. K., Bolstad, G. H. & Pélabon, C. Allometric constraints and the evolution of allometry. Evolution 68, 866–885 (2014).
    PubMed  Article  Google Scholar 

    37.
    Pélabon, C. et al. Evolution of morphological allometry. Ann. N. Y. Acad. Sci. 1320, 58–75 (2014).
    ADS  PubMed  Article  Google Scholar 

    38.
    Duellman, W. E., Marion, A. B. & Hedges, S. B. Phylogenetics, classification, and biogeography of the treefrogs (amphibia: anura: arboranae). Zootaxa 4104, 001–109 (2016).
    Article  Google Scholar 

    39.
    Kamilar, J. M. & Cooper, N. Phylogenetic signal in primate behaviour, ecology and life history. Phil. Trans. R. Soc. B. 368, 20120341 (2013).
    PubMed  Article  Google Scholar 

    40.
    Landis, M. J. & Schraiber, J. G. Pulsed evolution shaped modern vertebrate body sizes. Proc. Natl. Acad. Sci. U. S. A. 114, 13224–13229 (2017).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    41.
    Levy, D. L. & Heald, R. Biological scaling problems and solutions in amphibians. Cold Spring Harb. Perspect. Biol. 8, a019166 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    42.
    Boutilier, R. G., Stiffler, D. F. & Toews, D. Exchange of respiratory gases, ions, and water in amphibious and aquatic amphibians. In Environmental Physiology of Amphibians (eds Feder, M. E. & Burggren, W. W.) 81–124 (University of Chicago Press, Chicago, 1992).
    Google Scholar 

    43.
    Spotila, J. R., O’connor, M. P. & Bakken, G. S. Biophysics of heat and mass transfer. In Environmental Physiology of the Amphibians (eds Feder, M. E. & Burggren, W. W.) 59–80 (University of Chicago Press, Chicago, 1992).
    Google Scholar 

    44.
    Sanger, T. J. et al. Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67, 2180–2193 (2013).
    PubMed  Article  PubMed Central  Google Scholar 

    45.
    Navas, C. A., Antoniazzi, M. M. & Jared, C. A preliminary assessment of anuran physiological and morphological adaptation to the caatinga, a brazilian semi-arid environment. Int. Congr. Ser. 1275, 298–305 (2004).
    Article  Google Scholar 

    46.
    Wiley, D. F. et al. Evolutionary Morphing Minneapolis, MN, USA Minneapolis, MN, USA (IEEE Computer Society, Minneapolis, 2005).
    Google Scholar 

    47.
    Klingenberg, C. P. & Gidaszewski, N. A. Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Syst. Biol. 59, 245–261 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    48.
    Dryden, I. L. & Mardia, K. V. Statistical Shape Analysis (Wiley, Hoboken, 1998).
    Google Scholar 

    49.
    Adams, D. C. A generalized k statistic for estimating phylogenetic signal from shape and other high-dimenstional multivariate data. Syst. Biol. 63(5), 685–697 (2014).
    PubMed  Article  PubMed Central  Google Scholar 

    50.
    Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).
    PubMed  Article  Google Scholar 

    51.
    Adams, D. C. & Otárola-Castillo, E. Geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).
    Article  Google Scholar 

    52.
    Fox, J. & Hong, J. Effect displays in r for multinomial and proportional-odds logit models: extensions to the effects package. J. Stat. Softw. 32, 1–24 (2009).
    Article  Google Scholar 

    53.
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2016). More

  • in

    Aircraft events correspond with vocal behavior in a passerine

    1.
    Barber, J. R., Crooks, K. R. & Fristrup, K. M. The costs of chronic noise exposure for terrestrial organisms. Trends Ecol. Evol. 25, 180–189 (2010).
    PubMed  Article  Google Scholar 
    2.
    Buxton, R. T. et al. Noise pollution is pervasive in US protected areas. Science (80-) 356, 531–533 (2017).
    ADS  CAS  Article  Google Scholar 

    3.
    Manci, K. M., Gladwin, D. N., Villella, R. & Cavendish, M. G. Effects of aircraft noise and sonic booms on domestic animals and wildlife: a literature synthesis (Engineering and Services Center U. S. Air Force, 1988).

    4.
    Pott-Pollenske, M. et al. Airframe noise characteristics from flyover measurements and prediction. In 12th AIAA/CEAS Aeroacoustics Conference (27th AIAA Aeroacoustics Conference) 2567 (2006).

    5.
    Khardi, S. Reduction of commercial aircraft noise emission around airports. A new environmental challenge. Eur. Transp. Res. Rev. 1, 175–184 (2009).
    Article  Google Scholar 

    6.
    Dooling, R. J. & Popper, A. N. The effects of highway noise on birds (The California Department of Transportation Division of Environmental Analysis, 2007).

    7.
    Etzel, R. A. & Balk, S. J. Pediatric environmental health (American Academy of Pediatrics, Itasca, 2011).
    Google Scholar 

    8.
    Schomer, P. D. Growth function for human response to large-amplitude impulse noise. J. Acoust. Soc. Am. 64, 1627–1632 (1978).
    ADS  CAS  PubMed  Article  Google Scholar 

    9.
    Kunc, H. P. & Schmidt, R. The effects of anthropogenic noise on animals: a meta-analysis. Biol. Lett. 15, 20190649 (2019).
    PubMed  PubMed Central  Article  Google Scholar 

    10.
    Shannon, G. et al. A synthesis of two decades of research documenting the effects of noise on wildlife. Biol. Rev. 91, 982–1005 (2016).
    PubMed  Article  Google Scholar 

    11.
    Slabbekoorn, H. et al. A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol. Evol. 25, 419–427 (2010).
    PubMed  Article  Google Scholar 

    12.
    Brown, A. L. Measuring the effect of aircraft noise on sea birds. Environ. Int. 16, 587–592 (1990).
    Article  Google Scholar 

    13.
    McLaughlin, K. E. & Kunc, H. P. Experimentally increased noise levels change spatial and singing behaviour. Biol. Lett. 9, 20120771 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    14.
    Injaian, A. S., Poon, L. Y. & Patricelli, G. L. Effects of experimental anthropogenic noise on avian settlement patterns and reproductive success. Behav. Ecol. 29, 1181–1189 (2018).
    Article  Google Scholar 

    15.
    McClure, C. J. W., Ware, H. E., Carlisle, J., Kaltenecker, G. & Barber, J. R. An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road. Proc. R. Soc. London B Biol. Sci. 280, 20132290 (2013).
    Google Scholar 

    16.
    Kruger, D. J. D. & Du Preez, L. H. The effect of airplane noise on frogs: a case study on the Critically Endangered Pickersgill’s reed frog (Hyperolius pickersgilli). Ecol. Res. 31, 393–405 (2016).
    Article  Google Scholar 

    17.
    Melcon, M. L. et al. Blue whales respond to anthropogenic noise. PLoS ONE 7, e32681 (2012).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    18.
    Sierro, J., Schloesing, E., Pavón, I. & Gil, D. European blackbirds exposed to aircraft noise advance their chorus, modify their song and spend more time singing. Front. Ecol. Evol. 5, 68 (2017).
    Article  Google Scholar 

    19.
    McCarthy, E. et al. Changes in spatial and temporal distribution and vocal behavior of Blainville’s beaked whales (Mesoplodon densirostris) during multiship exercises with mid-frequency sonar. Mar. Mammal Sci. 27, E206–E226 (2011).
    Article  Google Scholar 

    20.
    Dominoni, D. M., Greif, S., Nemeth, E. & Brumm, H. Airport noise predicts song timing of European birds. Ecol. Evol. 6, 6151–6159 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    21.
    Gil, D., Honarmand, M., Pascual, J., Pérez-Mena, E. & Macías, G. C. Birds living near airports advance their dawn chorus and reduce overlap with aircraft noise. Behav. Ecol. 26, 435–443 (2014).
    Article  Google Scholar 

    22.
    Habib, L., Bayne, E. M. & Boutin, S. Chronic industrial noise affects pairing success and age structure of ovenbirds Seiurus aurocapilla. J. Appl. Ecol. 44, 176–184 (2007).
    Article  Google Scholar 

    23.
    Halfwerk, W., Holleman, L. J. M., Lessells, C. K. & Slabbekoorn, H. Negative impact of traffic noise on avian reproductive success. J. Appl. Ecol. 48, 210–219 (2011).
    Article  Google Scholar 

    24.
    Wolfenden, A. D., Slabbekoorn, H., Kluk, K. & de Kort, S. R. Aircraft sound exposure leads to song frequency decline and elevated aggression in wild chiffchaffs. J. Anim. Ecol. 88, 1720–1731 (2019).
    PubMed  Article  Google Scholar 

    25.
    Halfwerk, W. et al. Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl. Acad. Sci. 108, 14549–14554 (2011).
    ADS  CAS  PubMed  Article  Google Scholar 

    26.
    Blickley, J. L., Blackwood, D. & Patricelli, G. L. Experimental evidence for the effects of chronic anthropogenic noise on abundance of Greater Sage-Grouse at leks. Conserv. Biol. 26, 461–471 (2012).
    PubMed  Article  Google Scholar 

    27.
    Pepper, C. B., Nascarella, M. A. & Kendall, R. J. A review of the effects of aircraft noise on wildlife and humans, current control mechanisms, and the need for further study. Environ. Manag. 32, 418–432 (2003).
    Article  Google Scholar 

    28.
    Staicer, C. A., Spector, D. A. & Horn, A. G. The dawn chorus and other diel patterns in acoustic signaling. In Ecology and evolution of acoustic communication in birds, 426–453 (1996).

    29.
    Gil, D. & Llusia, D. The bird dawn chorus revisited. In Coding strategies in vertebrate acoustic communication 45–90 (Springer, Berlin, 2020).

    30.
    Warren, P. S., Katti, M., Ermann, M. & Brazel, A. Urban bioacoustics: It’s not just noise. Anim. Behav. 71, 491–502 (2006).
    Article  Google Scholar 

    31.
    Dooling, R. Avian hearing and the avoidance of wind turbines (University of Maryland, College Park, 2002).
    Google Scholar 

    32.
    Díaz, M., Parra, A. & Gallardo, C. Serins respond to anthropogenic noise by increasing vocal activity. Behav. Ecol. 22, 332–336 (2011).
    Article  Google Scholar 

    33.
    Gentry, K. E. & Luther, D. A. Spatiotemporal patterns of avian vocal activity in relation to urban and rural background noise. J. Ecoacoust. https://doi.org/10.22261/jea.z9tqh (2017).
    Article  Google Scholar 

    34.
    Cunnington, G. M. & Fahrig, L. Plasticity in the vocalizations of anurans in response to traffic noise. Acta Oecologica 36, 463–470 (2010).
    ADS  Article  Google Scholar 

    35.
    Kaiser, K. & Hammers, J. The effect of anthropogenic noise on male advertisement call rate in the neotropical treefrog, Dendropsophus triangulum. Behaviour 146, 1053–1069 (2009).
    Article  Google Scholar 

    36.
    Brumm, H. & Slater, P. J. B. Ambient noise, motor fatigue, and serial redundancy in chaffinch song. Behav. Ecol. Sociobiol. 60, 475–481 (2006).
    Article  Google Scholar 

    37.
    Meh, F. et al. Humpback whales Megaptera novaeangliae alter calling behavior in response to natural sounds and vessel noise. Mar. Ecol. Prog. Ser. 607, 251–268 (2018).
    Article  Google Scholar 

    38.
    Slabbekoorn, H. & Peet, M. Ecology: birds sing at a higher pitch in urban noise. Nature 424, 267 (2003).
    ADS  CAS  PubMed  Article  Google Scholar 

    39.
    Ríos-Chelén, A. A., Lee, G. C. & Patricelli, G. L. Anthropogenic noise is associated with changes in acoustic but not visual signals in red-winged blackbirds. Behav. Ecol. Sociobiol. 69, 1139–1151 (2015).
    Article  Google Scholar 

    40.
    Gross, K., Pasinelli, G. & Kunc, H. P. Behavioral plasticity allows short-term adjustment to a novel environment. Am. Nat. 176, 456–464 (2010).
    PubMed  Article  Google Scholar 

    41.
    Gentry, K. E., McKenna, M. F. & Luther, D. A. Evidence of suboscine song plasticity in response to traffic noise fluctuations and temporary road closures. Bioacoustics 27, 165–181 (2018).
    Article  Google Scholar 

    42.
    Conomy, J. T., Dubovsky, J. A., Collazo, J. A. & Fleming, W. J. Do black ducks and wood ducks habituate to aircraft disturbance?. J. Wildl. Manag. 62, 1135–1142 (1998).
    Article  Google Scholar 

    43.
    Neo, Y. Y., Hubert, J., Bolle, L. J., Winter, H. V. & Slabbekoorn, H. European seabass respond more strongly to noise exposure at night and habituate over repeated trials of sound exposure. Environ. Pollut. 239, 367–374 (2018).
    CAS  PubMed  Article  Google Scholar 

    44.
    Halfwerk, W., Both, C. & Slabbekoorn, H. Noise affects nest-box choice of 2 competing songbird species, but not their reproduction. Behav. Ecol. 27, 1592–1600 (2016).
    Article  Google Scholar 

    45.
    Ware, H. E., McClure, C. J. W., Carlisle, J. D. & Barber, J. R. A phantom road experiment reveals traffic noise is an invisible source of habitat degradation. Proc. Natl. Acad. Sci. 112, 12105–12109 (2015).
    ADS  CAS  PubMed  Article  Google Scholar 

    46.
    Williams, R., Erbe, C., Ashe, E., Beerman, A. & Smith, J. Severity of killer whale behavioral responses to ship noise: A dose–response study. Mar. Pollut. Bull. 79, 254–260 (2014).
    CAS  PubMed  Article  Google Scholar 

    47.
    Cynx, J., Lewis, R., Tavel, B. & Tse, H. Amplitude regulation of vocalizations in noise by a songbird Taeniopygia guttata. Anim. Behav. 56, 107–113 (1998).
    CAS  PubMed  Article  Google Scholar 

    48.
    Rushing, C. S., Ryder, T. B. & Marra, P. P. Quantifying drivers of population dynamics for a migratory bird throughout the annual cycle. Proc. R. Soc. B Biol. Sci. 283, 20152846 (2016).
    Article  CAS  Google Scholar 

    49.
    Stanley, C. Q. et al. Connectivity of wood thrush breeding, wintering, and migration sites based on range-wide tracking. Conserv. Biol. 29, 164–174 (2015).
    PubMed  Article  Google Scholar 

    50.
    Kleist, N. J., Guralnick, R. P., Cruz, A. & Francis, C. D. Anthropogenic noise weakens territorial response to intruder’s songs. Ecosphere 7, e01259 (2016).
    Article  Google Scholar 

    51.
    Ward, S., Speakman, J. R. & Slater, P. J. B. The energy cost of song in the canary, Serinus canaria. Anim. Behav. 66, 893–902 (2003).
    Article  Google Scholar 

    52.
    Nemeth, E. & Brumm, H. Birds and anthropogenic noise: are urban songs adaptive?. Am. Nat. 176, 465–475 (2010).
    PubMed  Article  Google Scholar 

    53.
    Oberweger, K. & Goller, F. The metabolic cost of birdsong production. J. Exp. Biol. 204, 3379–3388 (2001).
    CAS  PubMed  Google Scholar 

    54.
    Ophir, A. G., Schrader, S. B. & Gilooly, J. F. Energetic cost of calling: general constraints and species-specific differences. J. Evol. Biol. 23, 1564–1569 (2010).
    CAS  PubMed  Article  Google Scholar 

    55.
    Thomas, R. et al. The trade-off between singing and mass gain in a daytime-singing bird, the European robin. Behaviour 140, 387–404 (2003).
    Article  Google Scholar 

    56.
    Sheikh, P. A. & Uhl, C. Airplane noise: A pervasive disturbance in Pennsylvania Parks, USA. J. Sound Vib. https://doi.org/10.1016/j.jsv.2003.09.014 (2004).
    Article  Google Scholar 

    57.
    Burnham, K. P. & Anderson, D. R. Multimodel inference understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004).
    MathSciNet  Article  Google Scholar 

    58.
    Hurvich, C. M. & Tsai, C.-L. Regression and time series model selection in small samples. Biometrika 76, 297–307 (1989).
    MathSciNet  MATH  Article  Google Scholar  More