More stories

  • in

    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

  • 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

    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

  • 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

  • in

    Gut microbiome is affected by inter-sexual and inter-seasonal variation in diet for thick-billed murres (Uria lomvia)

    1.
    Kuwae, T. et al. Biofilm grazing in a higher vertebrate: The Western Sandpiper, Calidris mauri. Ecology 89, 599–606 (2008).
    PubMed  Article  PubMed Central  Google Scholar 
    2.
    Góngora, E., Braune, B. M. & Elliott, K. H. Nitrogen and sulfur isotopes predict variation in mercury levels in Arctic seabird prey. Mar. Pollut. Bull. 135, 907–914 (2018).
    PubMed  Article  CAS  Google Scholar 

    3.
    Ben-Yosef, M., Aharon, Y., Jurkevitch, E. & Yuval, B. Give us the tools and we will do the job: Symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. Proc. R. Soc. B Biol. Sci. 277, 1545–1552 (2010).
    CAS  Article  Google Scholar 

    4.
    Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L. & Gilbert, M. T. P. Do vertebrate gut metagenomes confer rapid ecological adaptation?. Trends Ecol. Evol. 31, 689–699 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    5.
    Lapanje, A., Zrimec, A., Drobne, D. & Rupnik, M. Long-term Hg pollution-induced structural shifts of bacterial community in the terrestrial isopod (Porcellio scaber) gut. Environ. Pollut. 158, 3186–3193 (2010).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    6.
    Lewis, W. B., Moore, F. R. & Wang, S. Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. J. Avian Biol. 47, 659–668 (2016).
    Article  Google Scholar 

    7.
    Bolnick, D. I. et al. Individuals’ diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol. Lett. 17, 979–987 (2014).
    PubMed  PubMed Central  Article  Google Scholar 

    8.
    Bolnick, D. I. et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 5, 4500 (2014).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    9.
    Bolnick, D. I., Yang, L. H., Fordyce, J. A., Davis, J. M. & Svanbäck, R. Measuring individual-level resource specialization. Ecology 83, 2936–2941 (2002).
    Article  Google Scholar 

    10.
    Bolnick, D. I. et al. The ecology of individuals: Incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).
    MathSciNet  PubMed  Article  PubMed Central  Google Scholar 

    11.
    Apajalahti, J. H. A., Kettunen, A., Bedford, M. R. & Holben, W. E. Percent G + C profiling accurately reveals diet-related differences in the gastrointestinal microbial community of broiler chickens. Appl. Environ. Microbiol. 67, 5656–5667 (2001).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    12.
    Apajalahti, J. & Kettunen, A. Microbes of the chicken gastrointestinal tract. In Avian Gut Function in Health and Disease (ed. Perry, G. C.) 124–137 (CAB International, Wallingford, 2006).
    Google Scholar 

    13.
    Oakley, B. B. et al. The chicken gastrointestinal microbiome. FEMS Microbiol. Lett. 360, 100–112 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    14.
    Bangert, R. L., Ward, A. C. S., Stauber, E. H., Cho, B. R. & Widders, P. R. A survey of the aerobic bacteria in the feces of captive raptors. Avian Dis. 32, 53–62 (1988).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    15.
    Soucek, Z. & Mushin, R. Gastrointestinal bacteria of certain Antarctic birds and mammals. Appl. Microbiol. 20, 561–566 (1970).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    16.
    Mead, G. C., Griffiths, N. M., Impey, C. S. & Coplestone, J. C. Influence of diet on the intestinal microflora and meat flavour of intensively-reared broiler chickens. Br. Poult. Sci. 24, 261–272 (1983).
    Article  Google Scholar 

    17.
    Waldenström, J. et al. Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds. Appl. Environ. Microbiol. 68, 5911–5917 (2002).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    18.
    Waite, D. W. & Taylor, M. W. Exploring the avian gut microbiota: Current trends and future directions. Front. Microbiol. 6, 1–12 (2015).
    Article  Google Scholar 

    19.
    Maul, J. D., Gandhi, J. P. & Farris, J. L. Community-level physiological profiles of cloacal microbes in songbirds (order: Passeriformes): Variation due to host species, host diet, and habitat. Microb. Ecol. 50, 19–28 (2005).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    20.
    Risely, A., Waite, D. W., Ujvari, B., Hoye, B. J. & Klaassen, M. Active migration is associated with specific and consistent changes to gut microbiota in Calidris shorebirds. J. Anim. Ecol. 87, 428–437 (2018).
    PubMed  Article  PubMed Central  Google Scholar 

    21.
    Dewar, M. L. et al. Interspecific variations in the gastrointestinal microbiota in penguins. Microbiologyopen 2, 195–204 (2013).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    22.
    Waite, D. W. & Taylor, M. W. Characterizing the avian gut microbiota: Membership, driving influences, and potential function. Front. Microbiol. 5, 1–12 (2014).
    Article  Google Scholar 

    23.
    Teyssier, A. et al. Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine. Sci. Total Environ. 612, 1276–1286 (2018).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    24.
    Hird, S. M., Sánchez, C., Carstens, B. C. & Brumfield, R. T. Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 6, 1403 (2015).
    PubMed  Article  PubMed Central  Google Scholar 

    25.
    Capunitan, D. C., Johnson, O., Terrill, R. S. & Hird, S. M. Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Mol. Ecol. 29, 829–847 (2020).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    26.
    Michel, A. J. et al. The gut of the finch: Uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome 6, 167 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    27.
    Elliott, K. H., Woo, K. J. & Gaston, A. J. Specialization in murres: The story of eight specialists. Waterbirds 32, 491–506 (2009).
    Article  Google Scholar 

    28.
    Woo, K. J., Elliott, K. H., Davidson, M., Gaston, A. J. & Davoren, G. K. Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J. Anim. Ecol. 77, 1082–1091 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    29.
    Elliott, K. H., Gaston, A. J. & Crump, D. Sex-specific behavior by a monomorphic seabird represents risk partitioning. Behav. Ecol. 21, 1024–1032 (2010).
    Article  Google Scholar 

    30.
    Paredes, R., Jones, I. & Boness, D. Parental roles of male and female thick-billed murres and razorbills at the Gannet Islands, Labrador. Behaviour 143, 451–481 (2006).
    Article  Google Scholar 

    31.
    Atwell, L., Hobson, K. A. & Welch, H. E. Biomagnification and bioaccumulation of mercury in an arctic marine food web: Insights from stable nitrogen isotope analysis. Can. J. Fish. Aquat. Sci. 55, 1114–1121 (1998).
    CAS  Article  Google Scholar 

    32.
    Carr, M. K. et al. Stable sulfur isotopes identify habitat-specific foraging and mercury exposure in a highly mobile fish community. Sci. Total Environ. 586, 338–346 (2017).
    ADS  CAS  PubMed  Article  Google Scholar 

    33.
    Peterson, B. J. & Fry, B. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18, 293–320 (1987).
    Article  Google Scholar 

    34.
    Song, S. J. et al. Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems 1, e00021-e116 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    35.
    Grond, K., Sandercock, B. K., Jumpponen, A. & Zeglin, L. H. The avian gut microbiota: Community, physiology and function in wild birds. J. Avian Biol. 49, e01788 (2018).
    Article  Google Scholar 

    36.
    Lawson, P. A., Collins, M. D., Falsen, E. & Foster, G. Catellicoccus marimammalium gen. nov., sp. nov., a novel Gram-positive, catalase-negative, coccus-shaped bacterium from porpoise and grey seal. Int. J. Syst. Evol. Microbiol. 56, 429–432 (2006).
    CAS  PubMed  Article  Google Scholar 

    37.
    Sinigalliano, C. D. et al. Multi-laboratory evaluations of the performance of Catellicoccus marimammalium PCR assays developed to target gull fecal sources. Water Res. 47, 6883–6896 (2013).
    CAS  PubMed  Article  Google Scholar 

    38.
    Ryu, H. et al. Comparison of gull feces-specific assays targeting the 16S rRNA genes of Catellicoccus marimammalium and Streptococcus spp. Appl. Environ. Microbiol. 78, 1909–1916 (2012).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    39.
    Koskey, A. M., Fisher, J. C., Traudt, M. F., Newton, R. J. & McLellan, S. L. Analysis of the gull fecal microbial community reveals the dominance of Catellicoccus marimammalium in relation to culturable enterococci. Appl. Environ. Microbiol. 80, 757–765 (2014).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    40.
    Lu, J., Santo Domingo, J. W., Lamendella, R., Edge, T. & Hill, S. Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl. Environ. Microbiol. 74, 3969–3976 (2008).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    41.
    Benskin, C. M. H., Rhodes, G., Pickup, R. W., Wilson, K. & Hartley, I. R. Diversity and temporal stability of bacterial communities in a model passerine bird, the zebra finch. Mol. Ecol. 19, 5531–5544 (2010).
    PubMed  Article  PubMed Central  Google Scholar 

    42.
    Kreisinger, J. et al. Temporal stability and the effect of transgenerational transfer on fecal microbiota structure in a long distance migratory bird. Front. Microbiol. 8, 1–19 (2017).
    Article  Google Scholar 

    43.
    Grond, K., Ryu, H., Baker, A. J., Santo Domingo, J. W. & Buehler, D. M. Gastro-intestinal microbiota of two migratory shorebird species during spring migration staging in Delaware Bay, USA. J. Ornithol. 155, 969–977 (2014).
    Article  Google Scholar 

    44.
    Santos, S. S. et al. Diversity of cloacal microbial community in migratory shorebirds that use the Tagus estuary as stopover habitat and their potential to harbor and disperse pathogenic microorganisms. FEMS Microbiol. Ecol. 82, 63–74 (2012).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    45.
    Laviad-Shitrit, S., Izhaki, I., Lalzar, M. & Halpern, M. Comparative analysis of intestine microbiota of four wild waterbird species. Front. Microbiol. 10, 1–13 (2019).
    Article  Google Scholar 

    46.
    Weigand, M. R., Ryu, H., Bozcek, L., Konstantinidis, K. T. & Santo Domingo, J. W. Draft genome sequence of Catellicoccus marimammalium, a novel species commonly found in gull feces. Genome Announc. 1, 12–13 (2013).
    Article  Google Scholar 

    47.
    Dewar, M. L. et al. Influence of fasting during moult on the faecal microbiota of penguins. PLoS ONE 9, e99996 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    48.
    Dewar, M. L., Arnould, J. P. Y., Krause, L., Dann, P. & Smith, S. C. Interspecific variations in the faecal microbiota of Procellariiform seabirds. FEMS Microbiol. Ecol. 89, 47–55 (2014).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    49.
    Roggenbuck, M. et al. The microbiome of New World vultures. Nat. Commun. 5, 5498 (2014).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    50.
    Potrykus, J., White, R. L. & Bearne, S. L. Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium. Proteomics 8, 2691–2703 (2008).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    51.
    Tsuchiya, C., Sakata, T. & Sugita, H. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett. Appl. Microbiol. 46, 071018031740002–000 (2007).
    Article  CAS  Google Scholar 

    52.
    Tegtmeier, D., Riese, C., Geissinger, O., Radek, R. & Brune, A. Breznakia blatticola gen. nov. sp. nov. and Breznakia pachnodae sp. nov., two fermenting bacteria isolated from insect guts, and emended description of the family Erysipelotrichaceae. Syst. Appl. Microbiol. 39, 319–329 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    53.
    Vandamme, P. et al. Ornithobacterium rhinotracheale gen. nov., sp. nov. isolated from the avian respiratory tract. Int. J. Syst. Bacteriol. 44, 24–37 (1994).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    54.
    Cerdà-Cuéllar, M. et al. Do humans spread zoonotic enteric bacteria in Antarctica?. Sci. Total Environ. 654, 190–196 (2019).
    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

    55.
    Anderson, M. J. & Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing?. Ecol. Monogr. 83, 557–574 (2013).
    Article  Google Scholar 

    56.
    Lott, C. A., Meehan, T. D. & Heath, J. A. Estimating the latitudinal origins of migratory birds using hydrogen and sulfur stable isotopes in feathers: Influence of marine prey base. Oecologia 134, 505–510 (2003).
    ADS  PubMed  Article  PubMed Central  Google Scholar 

    57.
    Góngora, E., Elliott, K. & Whyte, L. Dataset from Gut microbiome is affected by inter-sexual and inter-seasonal variation in diet for thick-billed murres (Uria lomvia). Mendeley Data v4, (2020).

    58.
    Eriksson, P., Mourkas, E., González-Acuna, D., Olsen, B. & Ellström, P. Evaluation and optimization of microbial DNA extraction from fecal samples of wild Antarctic bird species. Infect. Ecol. Epidemiol. 7, 1386536 (2017).
    PubMed  PubMed Central  Google Scholar 

    59.
    Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).
    CAS  PubMed  Article  PubMed Central  Google Scholar 

    60.
    Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2012).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    61.
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    62.
    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    63.
    Bokulich, N. A. et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6, 90 (2018).
    PubMed  PubMed Central  Article  Google Scholar 

    64.
    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    65.
    Braune, B. M., Gaston, A. J., Hobson, K. A., Gilchrist, H. G. & Mallory, M. L. Changes in food web structure alter trends of mercury uptake at two seabird colonies in the Canadian arctic. Environ. Sci. Technol. 48, 13246–13252 (2014).
    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

    66.
    Callahan, B. J., Sankaran, K., Fukuyama, J. A., McMurdie, P. J. & Holmes, S. P. Bioconductor workflow for microbiome data analysis: From raw reads to community analyses. F1000Research 5, 1492 (2016).
    PubMed  PubMed Central  Article  Google Scholar 

    67.
    Bokulich, N. A. et al. q2-longitudinal: Longitudinal and paired-sample analyses of microbiome data. mSystems 3, 1–9 (2018).
    Article  Google Scholar 

    68.
    Wilcoxon, F. Individual comparisons by Ranking methods. Biometrics Bull. 1, 80 (1945).
    Article  Google Scholar 

    69.
    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46 (2001).
    Google Scholar 

    70.
    Lozupone, C. & Knight, R. UniFrac: A new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2005).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    71.
    Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).
    Article  Google Scholar 

    72.
    Shannon, C. E. & Weaver, W. The Mathematical Theory of Communication (University of Illinois Press, Champaign, 1949).
    Google Scholar 

    73.
    Kruskal, W. H. & Wallis, W. A. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47, 583–621 (1952).
    MATH  Article  Google Scholar 

    74.
    Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253 (2006).
    MathSciNet  PubMed  PubMed Central  MATH  Article  Google Scholar 

    75.
    Legendre, P. & Legendre, L. Ordination in reduced space. In Numerical Ecology Vol. 24 (eds Legendre, P. & Legendre, L.) 425–520 (Elsevier, Amsterdam, 2012).
    Google Scholar 

    76.
    Vázquez-Baeza, Y., Pirrung, M., Gonzalez, A. & Knight, R. EMPeror: A tool for visualizing high-throughput microbial community data. Gigascience 2, 16 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    77.
    Vázquez-Baeza, Y. et al. Bringing the dynamic microbiome to life with animations. Cell Host Microbe 21, 7–10 (2017).
    PubMed  Article  CAS  Google Scholar 

    78.
    McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    79.
    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    80.
    McMurdie, P. J. & Holmes, S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    81.
    Mann, H. B. & Whitney, D. R. On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Stat. 18, 50–60 (1947).
    MathSciNet  MATH  Article  Google Scholar 

    82.
    Bartoń, K. MuMIn: Multi-Model Inference. (2019). More

  • in

    Identifying priority core habitats and corridors for effective conservation of brown bears in Iran

    1.
    Kopatz, A. et al. Connectivity and population subdivision at the fringe of a large brown bear (Ursus arctos) population in North Western Europe. Conserv. Genet. 13, 681–692 (2012).
    Article  Google Scholar 
    2.
    Mohammadi, A. & Kaboli, M. Evaluating wildlife–vehicle collision hotspots using kernel-based estimation: a focus on the endangered Asiatic cheetah in central Iran. Hum. Wildl. Interact. 10, 13 (2016).
    Google Scholar 

    3.
    Murphy, S. M. et al. Consequences of severe habitat fragmentation on density, genetics, and spatial capture–recapture analysis of a small bear population. PLoS ONE 12, e0181849 (2017).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    4.
    Hosseini-Zavarei, F., Farhadinia, M. S., Beheshti-Zavareh, M. & Abdoli, A. Predation by grey wolf on wild ungulates and livestock in central Iran. J. Zool. 290, 1–8 (2013).
    Article  Google Scholar 

    5.
    Tumendemberel, O. et al. Phylogeography, genetic diversity, and connectivity of brown bear populations in Central Asia. PLoS ONE 14, e0220746 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    6.
    Hilty, J. A., Lidicker, W. Z. Jr. & Merenlender, A. M. Corridor Ecology: The Science and Practice of Linking Landscapes for Biodiversity Conservation (Island Press, Washington, 2012).
    Google Scholar 

    7.
    Cushman, S. A. et al. Limiting factors and landscape connectivity: the American marten in the Rocky Mountains. Landsc. Ecol. 26, 1137 (2011).
    Article  Google Scholar 

    8.
    Oriol-Cotterill, A., Valeix, M., Frank, L. G., Riginos, C. & Macdonald, D. W. Landscapes of coexistence for terrestrial carnivores: the ecological consequences of being downgraded from ultimate to penultimate predator by humans. Oikos 124, 1263–1273 (2015).
    Article  Google Scholar 

    9.
    Cushman, S. A. et al. Prioritizing core areas, corridors and conflict hotspots for lion conservation in southern Africa. PLoS ONE 13, e0196213 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    10.
    Rio-Maior, H., Nakamura, M., Álvares, F. & Beja, P. Designing the landscape of coexistence: integrating risk avoidance, habitat selection and functional connectivity to inform large carnivore conservation. Biol. Conserv. 235, 178–188 (2019).
    Article  Google Scholar 

    11.
    Macdonald, D. W. et al. Multi-scale habitat modelling identifies spatial conservation priorities for mainland clouded leopards (Neofelis nebulosa). Divers. Distrib. 25, 1639–1654 (2019).
    Article  Google Scholar 

    12.
    Johansson, Ö. et al. Land sharing is essential for snow leopard conservation. Biol. Conserv. 203, 1–7 (2016).
    Article  Google Scholar 

    13.
    López-Bao, J. V., Bruskotter, J. & Chapron, G. Finding space for large carnivores. Nat. Ecol. Evol. 1, 1–2 (2017).
    Article  Google Scholar 

    14.
    Crespin, S. J. & Simonetti, J. A. Reconciling farming and wild nature: Integrating human–wildlife coexistence into the land-sharing and land-sparing framework. Ambio 48, 131–138 (2019).
    PubMed  Article  PubMed Central  Google Scholar 

    15.
    Kaszta, Ż, Cushman, S. A. & Macdonald, D. W. Prioritizing habitat core areas and corridors for a large carnivore across its range. Anim. Conserv. 23, 1–10 (2020).
    Article  Google Scholar 

    16.
    Kaszta, Ż et al. Simulating the impact of Belt and Road initiative and other major developments in Myanmar on an ambassador felid, the clouded leopard, Neofelis nebulosa. Landsc. Ecol. 35, 727–746 (2020).
    Article  Google Scholar 

    17.
    Cushman, S. A., Compton, B. W. & McGarigal, K. Habitat fragmentation effects depend on complex interactions between population size and dispersal ability: modeling influences of roads, agriculture and residential development across a range of life-history characteristics. In Spatial Complexity, Informatics, and Wildlife Conservation (eds Cushman, S. A. & Huettmann, F.) 369–385 (Springer, Berlin, 2010).
    Google Scholar 

    18.
    Kaszta, Ż et al. Integrating Sunda clouded leopard (Neofelis diardi) conservation into development and restoration planning in Sabah (Borneo). Biol. Conserv. 235, 63–76 (2019).
    Article  Google Scholar 

    19.
    Beier, P., Majka, D. R. & Spencer, W. D. Forks in the road: choices in procedures for designing wildland linkages. Conserv. Biol. 22, 836–851 (2008).
    PubMed  Article  PubMed Central  Google Scholar 

    20.
    Romportl, D. et al. Designing migration corridors for large mammals in the Czech Republic. J. Landsc. Ecol. 6, 47–62 (2013).
    Article  Google Scholar 

    21.
    Ruiz-González, A. et al. Landscape genetics for the empirical assessment of resistance surfaces: the European pine marten (Martes martes) as a target-species of a regional ecological network. PLoS ONE 9, e110552 (2014).
    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

    22.
    Cushman, S. A., Elliot, N. B., Macdonald, D. W. & Loveridge, A. J. A multi-scale assessment of population connectivity in African lions (Panthera leo) in response to landscape change. Landsc. Ecol. 31, 1337–1353 (2016).
    Article  Google Scholar 

    23.
    Linnell, J., Salvatori, V. & Boitani, L. Guidelines for population level management plans for large carnivores in Europe. A Large Carnivore Initiative for Europe (2008).

    24.
    Reljic, S. et al. Challenges for transboundary management of a European brown bear population. Glob. Ecol. Conserv. 16, e00488 (2018).
    Article  Google Scholar 

    25.
    Mateo Sanchez, M. C., Cushman, S. A. & Saura, S. Scale dependence in habitat selection: the case of the endangered brown bear (Ursus arctos) in the Cantabrian Range (NW Spain). Int. J. Geogr. Inf. Sci. 28, 1531–1546 (2014).
    Article  Google Scholar 

    26.
    Vergara, M., Cushman, S. A., Urra, F. & Ruiz-González, A. Shaken but not stirred: multiscale habitat suitability modeling of sympatric marten species (Martes martes and Martes foina) in the northern Iberian Peninsula. Landsc. Ecol. 31, 1241–1260 (2016).
    Article  Google Scholar 

    27.
    Ziółkowska, E. et al. Assessing differences in connectivity based on habitat versus movement models for brown bears in the Carpathians. Landsc. Ecol. 31, 1863–1882 (2016).
    Article  Google Scholar 

    28.
    Sarkar, M. S. et al. Multiscale statistical approach to assess habitat suitability and connectivity of common leopard (Panthera pardus) in Kailash Sacred Landscape, India. Spat. Stat. 28, 304–318 (2018).
    MathSciNet  Article  Google Scholar 

    29.
    Ashrafzadeh, M. R. et al. A multi-scale, multi-species approach for assessing effectiveness of habitat and connectivity conservation for endangered felids. Biol. Conserv. 245, 108523 (2020).
    Article  Google Scholar 

    30.
    McGarigal, K., Wan, H. Y., Zeller, K. A., Timm, B. C. & Cushman, S. A. Multi-scale habitat selection modeling: a review and outlook. Landsc. Ecol. 31, 1161–1175 (2016).
    Article  Google Scholar 

    31.
    Wasserman, T. N., Cushman, S. A., Shirk, A. S., Landguth, E. L. & Littell, J. S. Simulating the effects of climate change on population connectivity of American marten (Martes americana) in the northern Rocky Mountains, USA. Landsc. Ecol. 27, 211–225 (2012).
    Article  Google Scholar 

    32.
    Mateo-Sánchez, M. C. et al. A comparative framework to infer landscape effects on population genetic structure: Are habitat suitability models effective in explaining gene flow?. Landsc. Ecol. 30, 1405–1420 (2015).
    Article  Google Scholar 

    33.
    Zeller, K. A. et al. Are all data types and connectivity models created equal? Validating common connectivity approaches with dispersal data. Divers. Distrib. 24, 868–879 (2018).
    Article  Google Scholar 

    34.
    Cushman, S. A., Lewis, J. S. & Landguth, E. L. Why did the bear cross the road? Comparing the performance of multiple resistance surfaces and connectivity modeling methods. Diversity 6, 844–854 (2014).
    Article  Google Scholar 

    35.
    Adriaensen, F. et al. The application of ‘least-cost’modelling as a functional landscape model. Landsc. Urban Plan. 64, 233–247 (2003).
    Article  Google Scholar 

    36.
    McRae, B. H. Isolation by resistance. Evolution (N. Y.) 60, 1551–1561 (2006).
    Google Scholar 

    37.
    Cushman, S. A., McKelvey, K. S. & Schwartz, M. K. Use of empirically derived source–destination models to map regional conservation corridors. Conserv. Biol. 23, 368–376 (2009).
    PubMed  Article  PubMed Central  Google Scholar 

    38.
    Compton, B. W., McGarigal, K., Cushman, S. A. & Gamble, L. R. A resistant-kernel model of connectivity for amphibians that breed in vernal pools. Conserv. Biol. 21, 788–799 (2007).
    PubMed  Article  PubMed Central  Google Scholar 

    39.
    Panzacchi, M. et al. Predicting the continuum between corridors and barriers to animal movements using step selection functions and randomized shortest paths. J. Anim. Ecol. 85, 32–42 (2016).
    PubMed  Article  PubMed Central  Google Scholar 

    40.
    Cushman, S. A., Lewis, J. S. & Landguth, E. L. Evaluating the intersection of a regional wildlife connectivity network with highways. Mov. Ecol. 1, 12 (2013).
    PubMed  PubMed Central  Article  Google Scholar 

    41.
    Moqanaki, E. M. & Cushman, S. A. All roads lead to Iran: predicting landscape connectivity of the last stronghold for the critically endangered Asiatic cheetah. Anim. Conserv. 20, 29–41 (2017).
    Article  Google Scholar 

    42.
    Khosravi, R., Hemami, M. & Cushman, S. A. Multispecies assessment of core areas and connectivity of desert carnivores in central Iran. Divers. Distrib. 24, 193–207 (2018).
    Article  Google Scholar 

    43.
    Shahnaseri, G. et al. Contrasting use of habitat, landscape elements, and corridors by grey wolf and golden jackal in central Iran. Landsc. Ecol. 34, 1263–1277 (2019).
    Article  Google Scholar 

    44.
    Cushman, S. A. & Landguth, E. L. Ecological associations, dispersal ability, and landscape connectivity in the northern Rocky Mountains. In Research Paper RMRS-RP-90. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. vol. 90, 21 p (2012).

    45.
    McGarigal, K. & Cushman, S. A. Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecol. Appl. 12, 335–345 (2002).
    Article  Google Scholar 

    46.
    Cozzi, G. et al. Anthropogenic food resources foster the coexistence of distinct life history strategies: year-round sedentary and migratory brown bears. J. Zool. 300, 142–150 (2016).
    Article  Google Scholar 

    47.
    McLellan, B. N., Proctor, M. F., Huber, D. & Michel, S. Ursus arctos (amended version of 2017 assessment). The IUCN Red List of Threatened Species 2017: e. T41688A121229971 (2017).

    48.
    Penteriani, V. & Melletti, M. Bears of the World: Ecology, Conservation and Management (Cambridge University Press, Cambridge, 2020).
    Google Scholar 

    49.
    Wolf, C. & Ripple, W. J. Range contractions of the world’s large carnivores. R. Soc. Open Sci. 4, 170052 (2017).
    PubMed  PubMed Central  Article  ADS  Google Scholar 

    50.
    Garshelis, D. & McLellan, B. Are bear subspecies a thing of the past?. Int. Bear News 20, 9–10 (2011).
    Google Scholar 

    51.
    Hajjar, I. The Syrian bear still lives in Syria. Int. Bear News 20, 7–11 (2011).
    Google Scholar 

    52.
    Calvignac, S., Hughes, S. & Hänni, C. Genetic diversity of endangered brown bear (Ursus arctos) populations at the crossroads of Europe, Asia and Africa. Divers. Distrib. 15, 742–750 (2009).
    Article  Google Scholar 

    53.
    Ansari, M. & Ghoddousi, A. Water availability limits brown bear distribution at the southern edge of its global range. Ursus 29, 13–24 (2018).
    Article  Google Scholar 

    54.
    Ashrafzadeh, M. R., Kaboli, M. & Naghavi, M. R. Mitochondrial DNA analysis of Iranian brown bears (Ursus arctos) reveals new phylogeographic lineage. Mamm. Biol. 81, 1–9 (2016).
    Article  Google Scholar 

    55.
    Gutleb, B. & Ziaie, H. On the distribution and status of the Brown Bear, Ursus arctos, and the Asiatic Black Bear, U. thibetanus, Iran. Zool. Middle East 18, 5–8 (1999).
    Article  Google Scholar 

    56.
    Moqanaki, E. M., Jiménez, J., Bensch, S. & López-Bao, J. V. Counting bears in the Iranian Caucasus: remarkable mismatch between scientifically-sound population estimates and perceptions. Biol. Conserv. 220, 182–191 (2018).
    Article  Google Scholar 

    57.
    Yusefi, G. H., Faizolahi, K., Darvish, J., Safi, K. & Brito, J. C. The species diversity, distribution, and conservation status of the terrestrial mammals of Iran. J. Mammal. 100, 55–71 (2019).
    Article  Google Scholar 

    58.
    Almasieh, K., Rouhi, H. & Kaboodvandpour, S. Habitat suitability and connectivity for the brown bear (Ursus arctos) along the Iran–Iraq border. Eur. J. Wildl. Res. 65, 57 (2019).
    Article  Google Scholar 

    59.
    Nezami, B. & Farhadinia, M. S. Litter sizes of brown bears in the Central Alborz Protected Area, Iran. Ursus 22, 167–171 (2011).
    Article  Google Scholar 

    60.
    Darvishsefat, A. A. Atlas of Protected Areas of Iran. (Ravi, 2006).

    61.
    Atzeni, L. et al. Meta-replication, sampling bias, and multi-scale model selection: a case study on snow leopard (Panthera uncia) in western China. Ecol. Evol. 10, 7686–7712 (2020).
    PubMed  PubMed Central  Article  Google Scholar 

    62.
    Ambarli, H., Erturk, A. & Soyumert, A. Current status, distribution, and conservation of brown bear (Ursidae) and wild canids (gray wolf, golden jackal, and red fox; Canidae) in Turkey (2016).

    63.
    Brown, J. L. SDM toolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol. Evol. 5, 694–700 (2014).
    Article  Google Scholar 

    64.
    Evans, J. S. & Oakleaf, J. Geomorphometry and gradient metrics toolbox (ArcGIS 10.0) (2012).

    65.
    Ghorbanian, A. et al. Improved land cover map of Iran using Sentinel imagery within Google Earth Engine and a novel automatic workflow for land cover classification using migrated training samples. ISPRS J. Photogram. Remote Sens. 167, 276–288 (2020).
    Article  ADS  Google Scholar 

    66.
    Sanderson, E. W. et al. The human footprint and the last of the wild: the human footprint is a global map of human influence on the land surface, which suggests that human beings are stewards of nature, whether we like it or not. Bioscience 52, 891–904 (2002).
    Article  Google Scholar 

    67.
    Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
    Article  Google Scholar 

    68.
    Jueterbock, A. ‘MaxentVariableSelection’vignette. (2015).

    69.
    R Development Core, team. A Language ans Environment for Statistical Computing. R Found Stat. Comput. Vienna Austria 2, (2018).

    70.
    Naimi, B., Hamm, N. A. S., Groen, T. A., Skidmore, A. K. & Toxopeus, A. G. Where is positional uncertainty a problem for species distribution modelling?. Ecography (Cop.) 37, 191–203 (2014).
    Article  Google Scholar 

    71.
    Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).
    Article  Google Scholar 

    72.
    Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
    Google Scholar 

    73.
    Evans, J. S. & Cushman, S. A. Gradient modeling of conifer species using random forests. Landsc. Ecol. 24, 673–683 (2009).
    Article  Google Scholar 

    74.
    Wasserman, T. N., Cushman, S. A., Schwartz, M. K. & Wallin, D. O. Spatial scaling and multi-model inference in landscape genetics: Martes Americana in Northern Idaho. Landsc. Ecol. 25, 1601–1612 (2010).
    Article  Google Scholar 

    75.
    Cushman, S. A. & Lewis, J. S. Movement behavior explains genetic differentiation in American black bears. Landsc. Ecol. 25, 1613–1625 (2010).
    Article  Google Scholar 

    76.
    Cushman, S. A., Macdonald, E. A., Landguth, E. L., Malhi, Y. & Macdonald, D. W. Multiple-scale prediction of forest loss risk across Borneo. Landsc. Ecol. 32, 1581–1598 (2017).
    Article  Google Scholar 

    77.
    Zeller, K. A., McGarigal, K. & Whiteley, A. R. Estimating landscape resistance to movement: a review. Landsc. Ecol. 27, 777–797 (2012).
    Article  Google Scholar 

    78.
    Wan, H. Y., Cushman, S. A. & Ganey, J. L. Improving habitat and connectivity model predictions with multi-scale resource selection functions from two geographic areas. Landsc. Ecol. 34, 503–519 (2019).
    Article  Google Scholar 

    79.
    Landguth, E. L., Hand, B. K., Glassy, J., Cushman, S. A. & Sawaya, M. A. UNICOR: a species connectivity and corridor network simulator. Ecography (Cop.) 35, 9–14 (2012).
    Article  Google Scholar 

    80.
    Cushman, S. A., Landguth, E. L. & Flather, C. H. Evaluating population connectivity for species of conservation concern in the American Great Plains. Biodivers. Conserv. 22, 2583–2605 (2013).
    Article  Google Scholar 

    81.
    Kaszta, Ż, Cushman, S. A., Sillero-Zubiri, C., Wolff, E. & Marino, J. Where buffalo and cattle meet: modelling interspecific contact risk using cumulative resistant kernels. Ecography (Cop.) 41, 1616–1626 (2018).
    Article  Google Scholar 

    82.
    Støen, O.-G. Natal Dispersal and Social Organization in Brown Bears. (Norwegian University of Life Sciences, Department of Ecology and Natural, 2006).

    83.
    Saura, S. & Pascual-Hortal, L. A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc. Urban Plan. 83, 91–103 (2007).
    Article  Google Scholar 

    84.
    Saura, S. & Torné, J. Conefor Sensinode 2.2: a software package for quantifying the importance of habitat patches for landscape connectivity. Environ. Model. Softw. 24, 135–139 (2009).
    Article  Google Scholar 

    85.
    Avon, C. & Bergès, L. Prioritization of habitat patches for landscape connectivity conservation differs between least-cost and resistance distances. Landsc. Ecol. 31, 1551–1565 (2016).
    Article  Google Scholar 

    86.
    Ahmadi, M. et al. SPECIES OR SPACE: a combined gap analysis to guide management planning of conservation areas. Landsc. Ecol. 35, 1505–1517 (2020).
    Article  Google Scholar 

    87.
    Saura, S. & Rubio, L. A common currency for the different ways in which patches and links can contribute to habitat availability and connectivity in the landscape. Ecography (Cop.) 33, 523–537 (2010).
    Google Scholar 

    88.
    Elliot, N. B., Cushman, S. A., Macdonald, D. W. & Loveridge, A. J. The devil is in the dispersers: predictions of landscape connectivity change with demography. J. Appl. Ecol. 51, 1169–1178 (2014).
    Article  Google Scholar 

    89.
    Noroozi, J., Akhani, H. & Breckle, S.-W. Biodiversity and phytogeography of the alpine flora of Iran. Biodivers. Conserv. 17, 493–521 (2008).
    Article  Google Scholar 

    90.
    Habibzadeh, N. & Ashrafzadeh, M. R. Habitat suitability and connectivity for an endangered brown bear population in the Iranian Caucasus. Wildl. Res. 45, 602–610 (2018).
    Article  Google Scholar 

    91.
    Ashrafzadeh, M.-R., Khosravi, R., Ahmadi, M. & Kaboli, M. Landscape heterogeneity and ecological niche isolation shape the distribution of spatial genetic variation in Iranian brown bears, Ursus arctos (Carnivora: Ursidae). Mamm. Biol. 93, 64–75 (2018).
    Article  Google Scholar 

    92.
    Ash, E., Cushman, S. A., Macdonald, D. W., Redford, T. & Kaszta, Ż. How important are resistance, dispersal ability, population density and mortality in temporally dynamic simulations of population connectivity? A case study of tigers in southeast Asia. Land 9, 415 (2020).
    Article  Google Scholar 

    93.
    Cushman, S. A. et al. Biological corridors and connectivity [Chapter 21]. In Key Topics in Conservation Biology 2 (eds Macdonald, D. W. & Willis, K. J.) 384–404 (Wiley, Hoboken, 2013).
    Google Scholar 

    94.
    Ghoddousi, A. Habitat suitability modelling of the Brown bear Ursus arctos in Croatia and Slovenia using telemetry data (2010).

    95.
    Steyaert, S. M. J. G. et al. Ecological implications from spatial patterns in human-caused brown bear mortality. Wildl. Biol. 22, 144–152 (2016).
    Article  Google Scholar 

    96.
    Güthlin, D. et al. Estimating habitat suitability and potential population size for brown bears in the Eastern Alps. Biol. Conserv. 144, 1733–1741 (2011).
    Article  Google Scholar 

    97.
    Penteriani, V. et al. Evolutionary and ecological traps for brown bears Ursus arctos in human-modified landscapes. Mamm. Rev. 48, 180–193 (2018).
    Article  Google Scholar 

    98.
    Zarzo-Arias, A. et al. Identifying potential areas of expansion for the endangered brown bear (Ursus arctos) population in the Cantabrian Mountains (NW Spain). PLoS ONE 14, e0209972 (2019).
    CAS  PubMed  PubMed Central  Article  Google Scholar 

    99.
    Morales-González, A., Ruiz-Villar, H., Ordiz, A. & Penteriani, V. Large carnivores living alongside humans: brown bears in human-modified landscapes. Glob. Ecol. Conserv. 22, e00937 (2020).
    Article  Google Scholar 

    100.
    Fedorca, A. et al. Inferring fine-scale spatial structure of the brown bear (Ursus arctos) population in the Carpathians prior to infrastructure development. Sci. Rep. 9, 1–12 (2019).
    Article  CAS  Google Scholar 

    101.
    Liu, C., Newell, G., White, M. & Bennett, A. F. Identifying wildlife corridors for the restoration of regional habitat connectivity: a multispecies approach and comparison of resistance surfaces. PLoS ONE 13, e0206071 (2018).
    PubMed  PubMed Central  Article  CAS  Google Scholar 

    102.
    Macdonald, D. W. et al. Predicting biodiversity richness in rapidly changing landscapes: Climate, low human pressure or protection as salvation?. Biodivers. Conserv. 29, 4035–4057 (2020).
    Article  Google Scholar 

    103.
    Herrero, S., Smith, T., DeBruyn, T. D., Gunther, K. & Matt, C. A. From the field: brown bear habituation to people—safety, risks, and benefits. Wildl. Soc. Bull. 33, 362–373 (2005).
    Article  Google Scholar 

    104.
    Skuban, M. et al. Effects of roads on brown bear movements and mortality in Slovakia. Eur. J. Wildl. Res. 63, 82 (2017).
    Article  Google Scholar 

    105.
    Findo, S., Skuban, M., Kajba, M., Chalmers, J. & Kalaš, M. Identifying attributes associated with brown bear (Ursus arctos) road-crossing and roadkill sites. Can. J. Zool. 97, 156–164 (2019).
    Article  Google Scholar 

    106.
    Watson, J. E. M. et al. Persistent disparities between recent rates of habitat conversion and protection and implications for future global conservation targets. Conserv. Lett. 9, 413–421 (2016).
    Article  Google Scholar 

    107.
    Boitani, L., Ciucci, P., Corsi, F. & Dupre, E. Potential range and corridors for brown bears in the Eastern Alps. Italy. Ursus 11, 123–130 (1999).
    Google Scholar 

    108.
    Cushman, S. A., McKelvey, K. S., Hayden, J. & Schwartz, M. K. Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am. Nat. 168, 486–499 (2006).
    PubMed  Article  PubMed Central  Google Scholar 

    109.
    Mohammadi, A. et al. Road expansion: a challenge to conservation of mammals, with particular emphasis on the endangered Asiatic cheetah in Iran. J. Nat. Conserv. 43, 8–18 (2018).
    Article  Google Scholar  More

  • in

    The preference of Trichopria drosophilae for pupae of Drosophila suzukii is independent of host size

    1.
    DiGiacomo, G., Hadrich, J., Hutchison, W. D., Peterson, H. & Rogers, M. Economic impact of spotted wing drosophila (Diptera: Drosophilidae) yield loss on Minnesota Raspberry farms: A grower survey. J. Integr. Pest Manag. 10, https://doi.org/10.1093/jipm/pmz006 (2019).
    2.
    Farnsworth, D. et al. Economic analysis of revenue losses and control costs associated with the spotted wing drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Manag. Sci. 73, 1083–1090. https://doi.org/10.1002/ps.4497 (2017).
    CAS  Article  PubMed  Google Scholar 

    3.
    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 

    4.
    Okada, T. Systematic Study of Drosophilidae and Allied Families of Japan. 95–106 (Gihodo Co. Ltd., 1956).

    5.
    Walsh, D. B. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integr. Pest Manag. 2, G1–G7. https://doi.org/10.1603/Ipm10010 (2011).
    Article  Google Scholar 

    6.
    Kanzawa, T. Studies on Drosophila suzukii mats. J. Plant Proteom. 23, 66–70, 127–132, 183–191 (1939).

    7.
    Bolda, M. P. & Goodhue, R. E. Spotted wing Drosophila: Potential economic impact of a newly established pest. Agric. Resour. Econ. Updates Univ. Calif. Giannini Found. 13, 5–8, https://doi.org/10.1016/j.jff.2015.04.027 (2010).

    8.
    Schetelig, M. F. et al. Environmentally sustainable pest control options for Drosophila suzukii. J. Appl. Entomol. 142, 3–17. https://doi.org/10.1111/jen.12469 (2017).
    Article  Google Scholar 

    9.
    Lee, J. C. et al. Biological control of spotted-wing Drosophila (Diptera: Drosophilidae)—Current and pending tactics. J. Integr. Pest Manag. 10, https://doi.org/10.1093/jipm/pmz012 (2019).

    10.
    Fleury, F., Gibert, P., Ris, N. & Allemand, R. Chapter 1 Ecology and life history evolution of frugivorous Drosophila parasitoids. 70, 3–44, https://doi.org/10.1016/s0065-308x(09)70001-6 (2009).

    11.
    Daane, K. M. et al. First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J. Pest Sci. 89, 823–835. https://doi.org/10.1007/s10340-016-0740-0 (2016).
    ADS  Article  Google Scholar 

    12.
    Girod, P. et al. The parasitoid complex of D. suzukii and other fruit feeding Drosophila species in Asia. Sci. Rep. 8, 11839, https://doi.org/10.1038/s41598-018-29555-8 (2018).

    13.
    Girod, P. et al. Host specificity of Asian parasitoids for potential classical biological control of Drosophila suzukii. J. Pest. Sci. 2004(91), 1241–1250. https://doi.org/10.1007/s10340-018-1003-z (2018).
    Article  Google Scholar 

    14.
    Matsuura, A., Mitsui, H. & Kimura, M. T. A preliminary study on distributions and oviposition sites of Drosophila suzukii (Diptera: Drosophilidae) and its parasitoids on wild cherry tree in Tokyo, central Japan. Appl. Entomol. Zool. 53, 47–53. https://doi.org/10.1007/s13355-017-0527-7 (2018).
    Article  Google Scholar 

    15.
    Wang, X. G., Nance, A. H., Jones, J. M. L., Hoelmer, K. A. & Daane, K. M. Aspects of the biology and reproductive strategy of two Asian larval parasitoids evaluated for classical biological control of Drosophila suzukii. Biol. Control 121, 58–65. https://doi.org/10.1016/j.biocontrol.2018.02.010 (2018).
    Article  Google Scholar 

    16.
    Abram, P. K. et al. New records of Leptopilina, Ganaspis, and Asobara species associated with Drosophila suzukii in North America, including detections of L. japonica and G. brasiliensis. J. Hymenoptera Res. 78, 1–17, https://doi.org/10.3897/jhr.78.55026 (2020).

    17.
    Puppato, S., Grassi, A., Pedrazzoli, F., De Cristofaro, A. & Ioriatti, C. First report of Leptopilina japonica in Europe. Insects 11, https://doi.org/10.3390/insects11090611 (2020).

    18.
    Kacsoh, B. Z. & Schlenke, T. A. High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS One 7, e34721, https://doi.org/10.1371/journal.pone.0034721 (2012).

    19.
    Chabert, S., Allemand, R., Poyet, M., Eslin, P. & Gibert, P. Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol. Control 63, 40–47. https://doi.org/10.1016/j.biocontrol.2012.05.005 (2012).
    Article  Google Scholar 

    20.
    Nagaraja, H. in Biological Control of Insect Pests Using Egg Parasitoids (eds S. Sithanantham, Chandish R. Ballal, S. K. Jalali, & N. Bakthavatsalam) Chapter 8, 175–189 (Springer, 2013).

    21.
    Rossi Stacconi, M. V., Grassi, A., Ioriatti, C. & Anfora, G. Augmentative releases of Trichopria drosophilae for the suppression of early season Drosophila suzukii populations. BioControl 64, 9–19, https://doi.org/10.1007/s10526-018-09914-0 (2018).

    22.
    Rossi-Stacconi, M. V. et al. Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: Useful clues for control strategies. J. Pest Sci. 89, 689–700. https://doi.org/10.1007/s10340-016-0753-8 (2016).
    Article  Google Scholar 

    23.
    Mazzetto, F. et al. Drosophila parasitoids in northern Italy and their potential to attack the exotic pest Drosophila suzukii. J. Pest Sci. 89, 837–850. https://doi.org/10.1007/s10340-016-0746-7 (2016).
    Article  Google Scholar 

    24.
    Wang, X. G., Kacar, G., Biondi, A. & Daane, K. M. Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biol. Control 96, 64–71. https://doi.org/10.1016/j.biocontrol.2016.02.004 (2016).
    Article  Google Scholar 

    25.
    Kacar, G., Wang, X. G., Biondi, A. & Daane, K. M. Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments. PLoS ONE 12, e0183525. https://doi.org/10.1371/journal.pone.0183525 (2017).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    26.
    Zhu, C. J., Li, J., Wang, H., Zhang, M. & Hu, H. Y. Demographic potential of the pupal parasitoid Trichopria drosophilae (Hymenoptera: Diapriidae) reared on Drosophila suzukii (Diptera: Drosophilidae). J. Asia-Pac. Entomol. 20, 747–751. https://doi.org/10.1016/j.aspen.2017.04.008 (2017).
    Article  Google Scholar 

    27.
    Kruitwagen, A., Beukeboom, L. W. & Wertheim, B. Optimization of native biocontrol agents, with parasitoids of the invasive pest Drosophila suzukii as an example. Evol. Appl. 11, 1473–1497. https://doi.org/10.1111/eva.12648 (2018).
    Article  PubMed  PubMed Central  Google Scholar 

    28.
    Rossi Stacconi, M. V. et al. Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol. Control 117, 188–196, https://doi.org/10.1016/j.biocontrol.2017.11.013 (2018).

    29.
    Wolf, S., Boycheva-Woltering, S., Romeis, J. & Collatz, J. Trichopria drosophilae parasitizes Drosophila suzukii in seven common non-crop fruits. J. Pest Sci. 93, 627–638. https://doi.org/10.1007/s10340-019-01180-y (2019).
    Article  Google Scholar 

    30.
    Wang, X. G. et al. Thermal performance of two indigenous pupal parasitoids attacking the invasive Drosophila suzukii (Diptera: Drosophilidae). Environ. Entomol. 47, 764–772. https://doi.org/10.1093/ee/nvy053 (2018).
    Article  PubMed  Google Scholar 

    31.
    Rossi Stacconi, M. V. et al. Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biol. Control 112, 20–27, https://doi.org/10.1016/j.biocontrol.2017.06.003 (2017).

    32.
    Colombari, F., Tonina, L., Battisti, A. & Mori, N. Performance of Trichopria drosophilae (Hymenoptera: Diapriidae), a generalist parasitoid of Drosophila suzukii (Diptera: Drosophilidae), at low temperature. J. Insect Sci. 20, https://doi.org/10.1093/jisesa/ieaa039 (2020).

    33.
    Carton, Y., Bouletreau, M., Alphen, J. J. M. V. & Lenteren, J. C. V. in The Genetics and Biology of Drosophila Vol. 3 (eds M. Ashburner, H.L. Carson, & J.N. Thompson) Chap. 39, 348–394 (Academic Press, 1986).

    34.
    Wang, X. G., Kacar, G., Biondi, A. & Daane, K. M. Life-history and host preference of Trichopria drosophilae, a pupal parasitoid of spotted wing drosophila. Biocontrol 61, 387–397. https://doi.org/10.1007/s10526-016-9720-9 (2016).
    CAS  Article  Google Scholar 

    35.
    Boycheva Woltering, S., Romeis, J. & Collatz, J. Influence of the rearing host on biological parameters of Trichopria drosophilae, a potential biological control agent of Drosophila suzukii. Insects 10, https://doi.org/10.3390/insects10060183 (2019).

    36.
    Yi, C. et al. Life history and host preference of Trichopria drosophilae from Southern China, one of the effective pupal parasitoids on the Drosophila species. Insects 11, https://doi.org/10.3390/insects11020103 (2020).

    37.
    Lynch, Z. R., Schlenke, T. A. & de Roode, J. C. Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup. J. Evol. Biol. 29, 1016–1029. https://doi.org/10.1111/jeb.12842 (2016).
    CAS  Article  PubMed  Google Scholar 

    38.
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675. https://doi.org/10.1038/nmeth.2089 (2012).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    39.
    Otto, M. & Mackauer, M. The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri : Influence of variations in host quality on offspring growth and fitness. Oecologia 117, 353–364. https://doi.org/10.1007/s004420050668 (1998).
    ADS  Article  PubMed  Google Scholar 

    40.
    Friard, O., Gamba, M. & Fitzjohn, R. BORIS: A free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330. https://doi.org/10.1111/2041-210x.12584 (2016).
    Article  Google Scholar 

    41.
    Bates, D., Machler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).
    Article  Google Scholar 

    42.
    R: A Language and Environment for Statistical Computing (R, Vienna, 2008).

    43.
    Steidle, J. L. M. & van Loon, J. J. A. in Chemoecology of Insect Eggs and Egg Deposition (eds Monika Hilker & Torsten Meiners) 291–317 (Blackwell, 2003).

    44.
    Romani, R., Isidoro, N., Bin, F. & Vinson, S. B. Host recognition in the pupal parasitoid Trichopria drosophilae: A morpho-functional approach. Entomol. Exp. Appl. 105, 119–128. https://doi.org/10.1046/j.1570-7458.2002.01040.x (2002).
    CAS  Article  Google Scholar 

    45.
    Ballman, E. S., Collins, J. A. & Drummond, F. A. Pupation behavior and predation on Drosophila suzukii (Diptera: Drosophilidae) pupae in maine wild blueberry fields. J. Econ. Entomol. 110, 2308–2317. https://doi.org/10.1093/jee/tox233 (2017).
    Article  PubMed  Google Scholar 

    46.
    Carton, Y. Biologie de pimpla instigator (Ichneumonidae: Pimplinae). Entomol. Exp. Appl. 17, 265–278. https://doi.org/10.1111/j.1570-7458.1974.tb00344.x (1974).
    Article  Google Scholar 

    47.
    Vinson, S. B. Host selection by insect parasitoids. Annu. Rev. Entomol. 21, 109–133. https://doi.org/10.1146/annurev.en.21.010176.000545 (1976).
    Article  Google Scholar 

    48.
    Poyet, M. et al. Resistance of Drosophila suzukii to the larval parasitoids Leptopilina heterotoma and Asobara japonica is related to haemocyte load. Physiol. Entomol. 38, 45–53. https://doi.org/10.1111/phen.12002 (2013).
    Article  Google Scholar 

    49.
    Honti, V., Csordas, G., Kurucz, E., Markus, R. & Ando, I. The cell-mediated immunity of Drosophila melanogaster: Hemocyte lineages, immune compartments, microanatomy and regulation. Dev. Comp. Immunol. 42, 47–56. https://doi.org/10.1016/j.dci.2013.06.005 (2014).
    CAS  Article  PubMed  Google Scholar 

    50.
    Iacovone, A., Ris, N., Poirie, M. & Gatti, J. L. Time-course analysis of Drosophila suzukii interaction with endoparasitoid wasps evidences a delayed encapsulation response compared to D. melanogaster. PLoS One 13, e0201573, https://doi.org/10.1371/journal.pone.0201573 (2018).

    51.
    Bozler, J., Kacsoh, B. Z. & Bosco, G. Maternal priming of offspring immune system in Drosophila. G3 (Bethesda) 10, 165–175, https://doi.org/10.1534/g3.119.400852 (2020).

    52.
    Charnov, E. L., Los-den Hartogh, R. L., Jones, W. T. & van den Assem, J. Sex ratio evolution in a variable environment. Nature 289, 27–33, https://doi.org/10.1038/289027a0 (1981).

    53.
    Sandlan, K. Sex-ratio regulation in Coccygomimus-Turionella Linnaeus (Hymenoptera, Ichneumonidae) and its ecological implications. Ecol. Entomol. 4, 365–378. https://doi.org/10.1111/j.1365-2311.1979.tb00596.x (1979).
    Article  Google Scholar 

    54.
    King, B. H. Offspring sex-ratios in parasitoid wasps. Q. Rev. Biol. 62, 367–396. https://doi.org/10.1086/415618 (1987).
    Article  Google Scholar  More

  • in

    Quality of Pinus sp. pellets with kraft lignin and starch addition

    The fines content of the pellets, agglutinated with wheat starch and kraft lignin (both at 4%), was 125 higher and 75% lower than in the control, respectively (Table 1). The fines generation of the pellets in all treatments was lower than 1% (0.03 to 0.27%) and, therefore, they met the marketing standard EN 14961-232.
    Table 1 Fine content (%), hardness (%), bulk density (g m−3), apparent density (g m−3) by gravimetric method and apparent density (g m−3) by X-ray densitometry of Pinus wood pellets produced with different percentages of the additives (A) corn and wheat and kraft lignin and in the control.
    Full size table

    The lower values of the fines content of the pellets produced with kraft lignin are possibly due to the densification process of the pellet matrix with higher contents of this additive, generating pellets with better bonding characteristics between the particles and, consequently, less fines. In addition, lignin has a cementing action between the cells9 during the pressing process, and high temperature causes this compound to reach the glass transition stage, ensuring a strong bond between the particles8,33. Pellets with lower fines production during handling and transport should be preferred commercially34. The fines content increases with the moisture level of the material, causing cracks to exhaust gases, mainly water vapor, and, consequently, reducing their mechanical resistance during handling35. On the other hand, the low moisture content makes biomass compaction difficult, due to the water’s characteristic of helping the heat transfer and promoting lignin plasticization as a natural biomass binder36. The moisture content between 8 and 12% in the dry basis is ideal for reducing fines generation to within the European standard EN 14961-232.
    The hardness of the pellets was similar with the different percentages of corn starch, but it was higher with wheat starch (Table 1). The hardness increased by 22% when the percentage of kraft lignin reached 5%, in relation to the control. The hardness of the pellets with 3 and 5% of corn starch and 4% of kraft lignin was similar to the control.
    The similar hardness of the pellets with the different percentages of wheat starch confirms studies that binders can reduce the mechanical properties of pellets at a higher moisture content, because water takes the place of hydrogen bonds, affecting cohesion between the particles37. Higher hardness affects pellet length, because the higher the hardness, the greater the breaking strength after contact with the pelletizing press knife15. In addition, pellets with lower hardness have points for water ingress, increasing the moisture content and consequently the breaking point and causing higher fine generation38. The higher hardness of pellets produced with 5% kraft lignin is possibly due to the decrease of their hygroscopic equilibrium moisture, due to the hydrophobic character of this compound. The kraft lignin residue is a compound of C–C and C–O–C phenylpropane units with low water relationship39. In addition, the constant pressing temperature of 120 °C plasticizes kraft lignin as an adhesive, increasing particle contact and reducing expansion due to lower hygroscopicity, consequently increasing hardness40. Kraft lignin, as an additive, facilitates the use of this residue and confers better properties to pellets by increasing their mechanical strength13,14,15.
    The bulk density of pellets with 1% corn or wheat starches and 3% kraft lignin was higher than other mixtures (Table 1). The bulk density of kraft lignin pellets was higher than those with corn or wheat starch. The bulk density of pellets with 1% corn starch and 5% kraft lignin was lower than those with 3% lignin, which were denser than those with only wood (control).
    The higher bulk density values for 3% kraft lignin pellets may be associated with a higher amount of lignin in the mixture (wood + additive), which plasticizes more efficiently, generating a smooth and uniform texture in the pellets and improving their density. The pelletizing matrix temperature influences the durability and bulk density of pellets36, as lignin is a natural wood binder and requires temperatures above the glass transition (75–100 °C) to produce bonding between the particles. Temperatures above 90 °C improve pellet characteristics, and require lower compaction pressure at increasing compaction matrix temperatures4,41. The lower density values of wheat starch pellets may be due to the high moisture content of the steam generated during the high temperatures in the compaction process (120 °C), causing micro-cracks in the pellet structure and reducing its density35. Starch acts as a lubricating agent in the pelletizing process, facilitating the flow of raw material through the pelletizing matrix36. The bulk density of the pellets was greater than the minimum required by the European Marketing Standard EN 14961-232, equal to or greater than 0.60 g cm−3 in all treatments. This highlights the potential use of additives in pelletizing, which should be at most 2% relative to the dry mass of primary raw material.
    The apparent density of pellets varied in a fashion similar to that of bulk density (Table 1), with no effect from the type and amount of additive added to the particles mass, comparing the three different additives and considering the same proportion used, except for pellets produced with 3% wheat starch, with lower apparent density. The apparent density of pellets produced with 1 and 2% corn starch and 1, 3, 4 and 5% kraft lignin was higher, and the other treatments were similar to the control (Table 1). Lignin and corn starch promoted better connection between particles, favoring biomass compaction and increasing pellet density.
    The variation in the apparent density of the pellets, similar to that of bulk density between 1.15 g m−3 (3% wheat) and 1.23 g m−3 (3% lignin), is possibly due to the wheat starch gelatinization process starting at lower temperatures (± 70 °C) than that of corn starch (± 85 °C)42. This leads to the starch adhering to the pellet feeder system wall, reducing the proportion of additive that reaches the pelletizing matrix and consequently diminishing the unit density of the pellet. The higher apparent density of pellets produced with 1 and 2% corn starch and 1, 3, 4 and 5% kraft lignin is due to the lower rate of return of the pelletizing process and the higher molecular weight of the additives, influencing the pellet density7,36. Bulk density and apparent density determine pellet storage and transport conditions, and are directly related to energy density in those with 1 and 2% corn starch and 1, 3, 4 and 5% lignin, with higher density and a higher amount of energy per volume unit43.
    The apparent density of the pellets produced with additives and evaluated by X-ray densitometry ranged from 1.00 to 1.31 g m−3 in their longitudinal axis (Table 1), with the lowest value for pellets produced with 1% wheat starch, and the highest value with 1% corn starch.
    The lower apparent density values of wheat starch pellets can be associated with the presence of cracks (empty spaces), directly related to the susceptibility to rupture2. Low density peaks indicate small cracks that are attributed to a moisture content of the mixture or particle sizes inadequate for pelletizing4, affecting the physical properties of biomass densification44. The average apparent density of pellets is within the range established by the German standard DIN 51731, from 1.00 to 1.40 g m−345.
    Pellet density varied in longitudinal density profiles, with one uniform and one irregular pattern (Fig. 1). The apparent density variation of pellets produced without additives along the longitudinal axis (coefficient of variation of 5.29%) was higher. On the other hand, the apparent density variation of the profile (coefficient of variation of 4.19%) with additives was lower, showing greater cohesion between the particles and the additives. X-ray densitometry showed pellet density variations for all additives and in the control.
    Figure 1

    Longitudinal variation of pellet density with different proportions of the additives kraft lignin and corn and wheat starch.

    Full size image

    Uniform or irregular density patterns according to longitudinal pellet density profiles are due to variations in pellet internal density, which can be attributed to factors such as additive molecular weight, particle size, and temperature and pressure during pelletization46,47,48. Cracks are common in compacted material during pelletizing4,6, and can be attributed to inadequate pellet moisture content or particle sizes. The density of biomass varies with the moisture content44 and with the temperature strengthening the adhesion between the particles. Density profiles can explain the performance of pellets, whose cracks and high density variability affect their durability and final quality, since reductions in density are associated with cracks and, consequently, pellet breakage or rupture points, which can generate fines5. The apparent density of the pellets by gravimetric and X-ray densitometry, similar between treatments with additives, confirm that this technique, commonly used to evaluate the apparent density of materials and easier to apply than other methodologies, can be used to evaluate the quality of the pellets. Variations in the apparent density and longitudinal density profile obtained with the gravimetric and X-ray densitometry demonstrate that factors such as moisture, binder type, pressure and particle size interfere with the pelletizing process, causing variations in the material’s internal structure46,47. In addition, this technique accesses different parts of the pellet and therefore identifies point variations in the product density as reported for the 2% wheat starch pellet.
    In conclusion, the additives reduced the fines content and increased the hardness and density of the pellets. Therefore, they have the potential to produce pellets with greater resistance to the transport, storage and handling processes. Apparent density along the longitudinal axis of the pellets without starch was higher. The apparent density of pellets containing starch increased the cohesion between the particles and reduced the density variation as shown by their densitometric profiles. More