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    The temperature dependence of microbial community respiration is amplified by changes in species interactions

    Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).Article 
    CAS 

    Google Scholar 
    Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).Article 
    CAS 

    Google Scholar 
    Lopez-Urrutia, A., San Martin, E., Harris, R. P. & Irigoien, X. Scaling the metabolic balance of the oceans. Proc. Natl Acad. Sci. USA 103, 8739–8744 (2006).Article 
    CAS 

    Google Scholar 
    Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487, 472–476 (2012).Article 
    CAS 

    Google Scholar 
    Crowther, T. W. et al. Quantifying global soil carbon losses in response to warming. Nature 540, 104–108 (2016).Article 
    CAS 

    Google Scholar 
    Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018).Article 
    CAS 

    Google Scholar 
    Rivkin, R. B. & Legendre, L. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291, 2398–2400 (2001).Article 
    CAS 

    Google Scholar 
    Friedlingstein, P. et al. Uncertainties in CMIP5 climate projections due to carbon cycle feedbacks. J. Clim. 27, 511–526 (2014).Article 

    Google Scholar 
    Smith, T. P. et al. Community-level respiration of prokaryotic microbes may rise with global warming. Nat. Commun. 10, 5124 (2019).Article 

    Google Scholar 
    Antwis, R. E. et al. Fifty important research questions in microbial ecology. FEMS Microbiol. Ecol. 93, fix044 (2017).Bardgett, R. D., Freeman, C. & Ostle, N. J. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2, 805–814 (2008).Article 
    CAS 

    Google Scholar 
    Enquist, B. J. et al. Scaling from traits to ecosystems: developing a general trait driver theory via integrating trait-based and metabolic scaling theories. Adv. Ecol. Res. 52, 249–318 (2015).Article 

    Google Scholar 
    Allen, A. P., Gillooly, J. F. & Brown, J. H. Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19, 202–213 (2005).Article 

    Google Scholar 
    Schramski, J. R., Dell, A. I., Grady, J. M., Sibly, R. M. & Brown, J. H. Metabolic theory predicts whole-ecosystem properties. Proc. Natl Acad. Sci. USA 112, 2617–2622 (2015).Article 
    CAS 

    Google Scholar 
    Alster, C. J., Koyama, A., Johnson, N. G., Wallenstein, M. D. & von Fischer, J. C. Temperature sensitivity of soil microbial communities: an application of macromolecular rate theory to microbial respiration. J. Geophys. Res. Biogeosci. 121, 1420–1433 (2016).Article 

    Google Scholar 
    Yvon-Durocher, G. et al. Five years of experimental warming increases the biodiversity and productivity of phytoplankton. PLoS Biol. 13, e1002324 (2015).Article 

    Google Scholar 
    Garzke, J., Connor, S. J., Sommer, U. & O’Connor, M. I. Trophic interactions modify the temperature dependence of community biomass and ecosystem function. PLoS Biol. 17, e2006806 (2019).Foster, K. R. & Bell, T. Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22, 1845–1850 (2012).Article 
    CAS 

    Google Scholar 
    Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).Article 
    CAS 

    Google Scholar 
    Machado, D. et al. Polarization of microbial communities between competitive and cooperative metabolism. Nat. Ecol. Evol. 5, 195–203 (2021).Article 

    Google Scholar 
    Bradford, M. A. et al. Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation. Nat. Ecol. Evol. 3, 223–231 (2019).Article 

    Google Scholar 
    Garcia-Martin, E. E., McNeill, S., Serret, P. & Leakey, R. J. G. Plankton metabolism and bacterial growth efficiency in offshore waters along a latitudinal transect between the UK and Svalbard. Deep Sea Res. I 92, 141–151 (2014).Article 
    CAS 

    Google Scholar 
    Davidson, E. A., Richardson, A. D., Savage, K. E. & Hollinger, D. Y. A distinct seasonal pattern of the ratio of soil respiration to total ecosystem respiration in a spruce-dominated forest. Glob. Change Biol. 12, 230–239 (2006).Article 

    Google Scholar 
    Dutkiewicz, S., Follows, M. J. & Bragg, J. G. Modeling the coupling of ocean ecology and biogeochemistry. Glob. Biogeochem. Cycles 23, GB4017 (2009).Article 

    Google Scholar 
    Follows, M. J., Dutkiewicz, S., Ward, B. & Follett, C. in Microbial Ecology of the Oceans 3rd edn (eds Gasol, J. & Kirchman, D.) Ch. 12 (John Wiley, 2018).Letten, A. D. & Stouffer, D. B. The mechanistic basis for higher-order interactions and non-additivity in competitive communities. Ecol. Lett. 22, 423–436 (2019).Article 

    Google Scholar 
    Grilli, J., Barabás, G., Michalska-Smith, M. J. & Allesina, S. Higher-order interactions stabilize dynamics in competitive network models. Nature 548, 210–213 (2017).Article 
    CAS 

    Google Scholar 
    Maynard, D. S., Crowther, T. W. & Bradford, M. A. Competitive network determines the direction of the diversity–function relationship. Proc. Natl Acad. Sci. USA 114, 11464–11469 (2017).Article 
    CAS 

    Google Scholar 
    Fiegna, F., Moreno-Letelier, A., Bell, T. & Barraclough, T. G. Evolution of species interactions determines microbial community productivity in new environments. ISME J. 9, 1235–1245 (2015).Article 

    Google Scholar 
    Lawrence, D. et al. Species interactions alter evolutionary responses to a novel environment. PLoS Biol. 10, e1001330 (2012).Article 
    CAS 

    Google Scholar 
    Harcombe, W. R., Chacón, J. M., Adamowicz, E. M., Chubiz, L. M. & Marx, C. J. Evolution of bidirectional costly mutualism from byproduct consumption. Proc. Natl Acad. Sci. USA 115, 12000–12004 (2018).Article 
    CAS 

    Google Scholar 
    Goldford, J. E. et al. Emergent simplicity in microbial community assembly. Science 361, 469–474 (2018).Article 
    CAS 

    Google Scholar 
    Yvon-Durocher, G. et al. Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507, 488–491 (2014).Article 
    CAS 

    Google Scholar 
    Fox, J. W. & Harpole, W. S. Revealing how species loss affects ecosystem function: the trait-based price equation partition. Ecology 89, 269–279 (2008).Article 

    Google Scholar 
    Kontopoulos, D., Smith, T. P., Barraclough, T. G. & Pawar, S. Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate. PLoS Biol. 18, e3000894 (2020).Article 
    CAS 

    Google Scholar 
    Wilson, W. G. & Lundberg, P. Biodiversity and the Lotka–Volterra theory of species interactions: open systems and the distribution of logarithmic densities. Proc. R. Soc. Lond. B 271, 1977–1984 (2004).Article 

    Google Scholar 
    Rossberg, A. G. in Food Webs and Biodiversity 181–191 (John Wiley & Sons, 2013).Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541 (2009).Article 
    CAS 

    Google Scholar 
    Garcia, F. C., Bestion, E., Warfield, R. & Yvon-Durocher, G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc. Natl Acad. Sci. USA 115, 10989–10999 (2018).Article 
    CAS 

    Google Scholar 
    Padfield, D., O’Sullivan, H. & Pawar, S. rTPC and nls.multstart: a new pipeline to fit thermal performance curves in R. Methods Ecol. Evol. 12, 1138–1143 (2021).Article 

    Google Scholar  More

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    A high-resolution gridded grazing dataset of grassland ecosystem on the Qinghai–Tibet Plateau in 1982–2015

    Study areaThe Qinghai–Tibet Plateau (26°00′-39°47′N, 73°19′-104°47′E), one of the most important pastoral areas in the world, straddles the southwest regions of China, and it includes 244 counties, which belong to six provinces: Tibet, Qinghai, Xinjiang, Gansu, Sichuan, and Yunnan. It is characterized by rich natural grassland resources, including desert steppes, alpine steppes, and alpine meadows (Fig. 1a). The grassland areas account for over 56% of this region34. The grassland plays a vital role in providing regional and national animal husbandry products and fodder35, which enables the local herders to obtain almost all of the resources required for survival36. The grazing density distribution is extremely unbalanced (Fig. 1a) owing to the high spatial heterogeneity of economic development (Fig. 1b-1) and grassland production (Fig. 1b-2), resulting from the differences in resources and environmental factors37. Over the past few decades, there has been a significant change in the number of livestock animals, and the number of sheep exceeded 160 million by 2020. Therefore, it is urgent to obtain a high-resolution gridded grazing dataset for its evaluating spatiotemporal changes and coordinating the relationship between human beings and the grassland ecosystem.Fig. 1Location of the Qinghai–Tibet Plateau: (a) grassland type and distribution, and grazing density (GD) in 244 counties; (b) spatial heterogeneity of economic development (ED) and grassland production (GP) in 244 counties. GD, ED, and GP are represented by sheep unit per grassland area per county (SU/hm2), human footprint index per pixel (HF/pixel) per county, and net primary production per grassland area per county (gC/m2), respectively.Full size imageFig. 2Methodological framework for grazing spatialization.Full size imageMethodological frameworkWe developed a methodological framework for high-resolution gridded grazing dataset mapping. The framework mainly includes four parts: (i) identifying features affecting grazing, (ii) extracting theoretical suitable grazing areas, (iii) building grazing spatialization model, and (iv) correcting the grazing spatialization dataset. Each step is explained in more detail below (Fig. 2).Step 1: Identifying features affecting grazingGrazing activities are affected by the spatial heterogeneity of resources and environmental factors, regulated by the grazing behavior of herders and the foraging behavior of herds, and restricted by ecological protection policies. Therefore, the specific implications of the 14 influencing factors from the above four aspects are presented in Table 1. These factors are necessary for spatializing the county-level grazing data.Table 1 The identified features affecting grazing.Full size tableStep 2: Extracting theoretical suitable grazing areasThe decision tree approach38 was adopted to extract the theoretical suitable grazing areas for further grazing spatialization (step 2 in Fig. 2). First, the potential grazing area was identified according to the boundary of the grassland ecosystem, because grazing behavior only occurs in the grassland. Then, the unsuitable areas for grazing, i.e., extremely-high-altitude areas and areas adjacent to towns, were removed from the potential grazing area stepwise. The areas strictly prohibited for grazing, i.e., the core areas of national nature reserves39 within grassland areas, were also deemed unsuitable for grazing. Finally, the extracted areas were the theoretically suitable grazing areas.Step 3: Building grazing spatialization model(i) Extracting cross-scale feature (CSFs)In the traditional method, the spatial resolution of the training data (i.e., the average value at the administrative level) differs from that of the predicting data (i.e., the value at the pixel level), and the trained model can only capture the characteristics within the training data. However, the extreme value of the predicting data inevitably exceeds the range of the training data, which can result in underestimation in these parts40. To reduce these mismatches, we built an improved method for CSFs extraction (Fig. 2, first part of step 3).First, the census grazing data are simply distributed from county level to pixel level using the weight of the absolute disturbance (AD) index as Eq. (1). The AD index is measured by Mahalanobis distance using Eq. (2), which is calculated according to the deviation between the potential and observed normalized difference vegetation index (NDVI) values22. Second, the distributed grazing data are graded via the hierarchical clustering method, and the optimal number of the group can be determined using the Davies–Bouldin index (DBI)41 as Eq. (3), an index for evaluating the quality of clustering algorithm. The smaller the DBI, the smaller the distance within each group. Therefore, the DBI can be used to select the best similar values to minimize the deviation within each group. Finally, we can obtain the scope of the groups within each county using the above two steps and obtain the average value of all independent variables and the dependent variable accordingly. As expected, we can decompose the average value at the county level (traditional features in Fig. 2) into the average value at the group level (improved features in Fig. 2).$$S{U}_{i}=S{U}_{j}^{C}frac{{w}_{A{D}_{i}}}{{w}_{A{D}_{j}}}$$
    (1)
    where SUi and (S{U}_{j}^{C}) are the grazing value for pixel i and the census grazing value for county j; ({w}_{A{D}_{i}}) is the weight of the AD index for pixel i and ({w}_{A{D}_{j}}) represents the summed weight of the AD index values for all pixels in county j.$$begin{array}{cll}A{D}_{i} & = & sqrt{{({D}_{i}-u)}^{T}co{v}^{-1}({D}_{i}-u)}\ {D}_{i} & = & NDV{I}_{i}^{T}-NDV{I}_{i}^{P}end{array}$$
    (2)
    where ADi is the AD index for pixel i; the vector composed of its observed NDVI (left(NDV{I}_{i}^{T}right)) and potential NDVI (left(NDV{I}_{i}^{P}right)) time-series data could be considered as two points in the feature space for pixel i, and Di and u are the difference and the mean value of the vector, respectively; cov is the covariance matrix.$$DB{I}_{k}=frac{1}{k}{sum }_{x=1}^{k}ma{x}_{yne x}left(frac{overline{{a}_{x}}+overline{{a}_{y}}}{left|{delta }_{x}-{delta }_{y}right|}right)$$
    (3)
    where DBIk is the DBI coefficient when the cluster number is k; (overline{{a}_{x}}) and (overline{{a}_{y}}) are the average distances of the group xth and the group yth, respectively; δx and δy are the center distance of the group xth and the group yth, respectively.Different from the traditional method, our method can decompose features into multiple features using the grading AD index. The differences among counties will not be easily averaged out. Moreover, our method is less affected by scale mismatch and can be transferred to cross-scale modeling26.(ii) Building RF model with partitioningA single model cannot accurately obtain the variation information of the Qinghai–Tibet Plateau with high spatial heterogeneity. The partition model, a widely used method for estimating population distribution and others42,43, can be incorporated into the proposed model to improve its performance. The thresholds (0.43, 0.35 and 0.21 SU/hm2), determined according to the theoretical livestock carrying capacity (equation S1), were calculated and used to separate independent variables and dependent variable for each grassland types: alpine meadow, alpine steppe and alpine desert steppe (see Section 6.1 for details). Then, the RF models were established, and the training and testing samples were randomly divided in the proportion of 3:1. It is notable that transforming the response variable using natural log prior to RF model fitting is necessary to achieve higher prediction accuracies44. Finally, the independent variables at the pixel level were inputted into the two trained RF models, and the corresponding grid grazing dataset was output by combining the two results (Fig. 2, second part of step 3).(iii) Validating the accuracy of the methodsThe performance of the grazing spatialization model was evaluated through a comparison of the predicted value with census value26. Accuracy validation indexes, including coefficients of determination (R2), root mean square error (RMSE), and mean absolute error (MAE), were used to evaluate the performances of the proposed RF-based models (Table 2), as presented in Eq. (4).$$begin{array}{ccc}{R}^{2} & = & 1-frac{{sum }_{j=1}^{N}{left(S{U}_{j}^{C}-S{U}_{j}^{P}right)}^{2}}{{sum }_{j=1}^{N}{left(S{U}_{j}^{C}-overline{S{U}^{C}}right)}^{2}}\ RMSE & = & sqrt{frac{{sum }_{j=1}^{N}{left(S{U}_{j}^{C}-S{U}_{j}^{P}right)}^{2}}{N}}\ MAE & = & frac{{sum }_{j=1}^{N}| S{U}_{j}^{C}-S{U}_{j}^{P}| }{N}end{array}$$
    (4)
    where (S{U}_{j}^{C}) and (S{U}_{j}^{P}) are the census grazing value and the predicted grazing value for county j, respectively; (overline{S{U}^{C}}) is the average census data for all counties; and N is the number of all counties.Table 2 The proposed methods and their descriptions.Full size tableStep 4: Correcting grazing spatialization dataset(i) Correcting residuals of datasetCorrecting residuals is necessary to obtain datasets with higher accuracy45,46, because propagating the cross-scale relationship in the RF models will inevitably generate errors47. The residuals, calculated by the difference between the average census grazing and predicted grazing values at the administrative level, were used to calibrate the errors related to all pixels within this county. The revised dataset after residual correction is the final product provided in this study. The residual correction method is expressed by Eq. (5), and the process is shown in the fourth step in Fig. 2.$$S{U}_{i}^{RP}=S{U}_{i}^{P}+{R}_{j}$$
    (5)
    where (S{U}_{i}^{RP}) denotes the predicted grazing value revised by the residuals for pixel i, (S{U}_{i}^{P}) denotes the predicted grazing for pixel i, and Rj denotes the residuals calculated from the difference between census grazing and predicted grazing data for county j.(ii) Validating the accuracy of datasetTwo goodness-of-fit indexes were used to validate the consistency of spatial distribution and the temporal trend between predicted grazing data and census grazing data. Generally, the coefficient of determination (R2), defined in Eq. (4), is used to verify the consistency of spatial distribution, and the Nash–Sutcliffe efficiency (NSE, Eq. (6)) is used to verify the consistency of temporal trend. An index value closer to 1 corresponds to a more accurate dataset. Meanwhile, we also collected field grazing data from 56 sites to further validate the spatial accuracy of the dataset, and it measured using the R2 in Eq. (4).$$NSE=1-frac{{sum }_{t=1}^{T}{left(S{U}_{t}^{RP}-S{U}_{t}^{C}right)}^{2}}{{sum }_{t=1}^{T}{left(S{U}_{t}^{C}-overline{S{U}^{{C}^{{prime} }}}right)}^{2}}$$
    (6)
    where (S{U}_{t}^{RP}) and (S{U}_{t}^{C}) are the predicted grazing value revised by residuals and the census grazing value of all counties in year t, respectively; (overline{S{U}^{{C}^{{prime} }}}) is the average census grazing value of all years; and T is the number of time steps.(iii) Identifying uncertainties associated with datasetThe uncertainties associated with the dataset originate from the following two aspects: First, the unreasonableness of our method, owing to the errors related to cross-scale modeling or the inappropriate selection of influencing factors, is an important source of uncertainties. Second, the incompleteness of auxiliary variables also introduces uncertainties. In this instance, grassland-free areas are not accurately identified in some counties, but livestock animals are raised in these counties. These counties have no effective value for livestock density prediction. Overall, the uncertainties can be identified in terms of the mean relative error (MRE) in Eq. (7).$$MRE=frac{{sum }_{j=1}^{N}left|frac{S{U}_{j}^{C}-S{U}_{j}^{RP}}{S{U}_{j}^{C}}right|}{N}ast 100 % $$
    (7)
    where (S{U}_{j}^{C}) is the census grazing value for county j, (S{U}_{j}^{RP}) is the predicted grazing value revised by residuals for county j, and N is the number of counties.Data sourceCensus grazing data at county levelEight types of livestock, namely cattle, yaks, horses, donkeys, mules, camels, goats, and sheep, were considered according to the regional characteristics, and livestock stocking quantity at the end of year for each county can be determined from statistical yearbooks. However, the numbers of livestock at the county level for some years between 1982 and 2015 were not recorded. The missing data were indirectly approximated from city- or provincial-level data (e.g., interpolation using their temporal trends). Each type of livestock stocking quantity was converted into standard sheep unit (SU) according to the national standards using Eq. (8)48, namely the calculation of rangeland carrying capacity (NY/T 635-2015). Of the 244 counties of the Qinghai–Tibet Plateau, only 242 counties were considered, as the census grazing data for the other 2 counties were unavailable. The unit of grazing statistics data at the county level is defined as SU per county per year (SU·county−1·year−1).$$begin{array}{l}SU={N}_{sheep}+0.8times {N}_{goats}+5times {N}_{cattle}+5times {N}_{yaks+}+\ 6times {N}_{horses}+3times {N}_{donkeys}+6times {N}_{mules}+7times {N}_{camels}end{array}$$
    (8)
    where Nsheep, Ngoats, Ncattle, Nyaks, Nhorses, Ndonkeys, Nmules, Ncamels are the number of sheep, goats, cattle, yaks, horses, donkeys, mules, and camels at the year-end, respectively. SU denotes the standard sheep unit (SU·county−1·year−1).Data of grazing influencing factors at pixel levelThe types of features affecting grazing were obtained from the first step described in Methods, and the detailed information, such as original spatiotemporal resolution, format, and source, is shown in Table 3. The format (i.e., GeoTIFF), spatial resolution (i.e., 0.083°), and the number of rows and columns of the gridded features were leveraged to further produce a high-resolution grazing dataset.Table 3 Data source of grazing influence factors.Full size table More

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    Salp blooms drive strong increases in passive carbon export in the Southern Ocean

    Roemmich, D. et al. Unabated planetary warming and its ocean structure since 2006. Nat. Clim. Change 5, 240–245 (2015).Article 
    ADS 

    Google Scholar 
    Frölicher, T. L. et al. Dominance of the Southern Ocean in anthropogenic carbon and heat uptake in CMIP5 models. J. Clim. 28, 862–886 (2015).Article 
    ADS 

    Google Scholar 
    Buesseler, K. O. & Boyd, P. W. Shedding light on processes that control particle export and flux attenuation in the twilight zone of the open ocean. Limnol. Oceanogr. 54, 1210–1232 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Arteaga, L., Haentjens, N., Boss, E., Johnson, K. S. & Sarmiento, J. L. Assessment of export efficiency equations in the Southern Ocean applied to satellite-based net primary production. J. Geophys. Res.-Oceans 123, 2945–2964 (2018).Article 
    ADS 

    Google Scholar 
    Siegel, D. A. et al. Prediction of the export and fate of global ocean net primary production: the EXPORTS science plan. Front. Marine Sc. 3, 22 (2016).Perissinotto, R. & Pakhomov, E. A. The trophic role of the tunicate Salpa thompsoni in the Antarctic marine ecosystem. J. Mar. Syst. 17, 361–374 (1998).Article 

    Google Scholar 
    Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432, 100–103 (2004).Article 
    ADS 
    CAS 

    Google Scholar 
    Perissinotto, R. & Pakhomov, E. A. Contribution of salps to carbon flux of marginal ice zone of the Lazarev sea, southern ocean. Mar. Biol. 131, 25–32 (1998).Article 
    CAS 

    Google Scholar 
    Phillips, B., Kremer, P. & Madin, L. P. Defecation by Salpa thompsoni and its contribution to vertical flux in the Southern Ocean. Mar. Biol. 156, 455–467 (2009).Article 

    Google Scholar 
    Stone, J. P. & Steinberg, D. K. Salp contributions to vertical carbon flux in the Sargasso Sea. Deep-Sea Res. Part I 113, 90–100 (2016).Article 
    CAS 

    Google Scholar 
    Ramaswamya, V., Sarin, M. M. & Rengarajan, R. Enhanced export of carbon by salps during the northeast monsoon period in the northern Arabian Sea. Deep-Sea Res. Part II 52, 1922–1929 (2005).Article 
    ADS 

    Google Scholar 
    Smith, K. L. et al. Large salp bloom export from the upper ocean and benthic community response in the abyssal northeast Pacific: day to week resolution. Limnol. Oceanogr. 59, 745–757 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Madin, L. P. & Kremer, P. Determination of the filter feeding rates of salps (Tunicata, Thaliacea). ICES J. Mar. Sci. 52, 583–595 (1995).Article 

    Google Scholar 
    Wiebe, P. H., Madin, L. P., Haury, L. R., Harbison, G. R. & Philbin, L. M. Diel vertical migration by Salpa aspera and its potential for large-scale particulate organic matter transport to the deep-sea. Mar. Biol. 53, 249–255 (1979).Article 

    Google Scholar 
    Dadon-Pilosof, A., Lombard, F., Genin, A., Sutherland, K. R. & Yahel, G. Prey taxonomy rather than size determines salp diets. Limnol. Oceanogr. 64, 1996–2010 (2019).Article 
    ADS 

    Google Scholar 
    Stukel, M. R., Décima, M., Selph, K. E. & Gutiérrez-Rodríguez, A. Size-specific grazing and competitive interactions between large salps and protistan grazers. Limnol. Oceanogr. 66, 2521–2534 (2021).Madin, L. P. Production, composition and sedimentation of salp fecal pellets in oceanic waters. Mar. Biol. 67, 39–45 (1982).Article 

    Google Scholar 
    Michaels, A. F. & Silver, M. W. Primary production, sinking fluxes and the microbial food web. Deep-Sea Res. Part I 35, 473–490 (1988).Article 
    ADS 

    Google Scholar 
    Luo, J. Y. et al. Gelatinous zooplankton‐mediated carbon flows in the global oceans: a data‐driven modeling study. Glob. Biogeochem. Cycle 34, e2020GB006704 (2020).Kremer, P. & Madin, L. P. Particle retention efficiency of salps. J. Plankton Res. 14, 1009–1015 (1992).Article 

    Google Scholar 
    Harbison, G. R. & Gilmer, R. W. Feeding rates of pelagic tunicate Pegea confederata and 2 other salps. Limnol. Oceanogr. 21, 517–528 (1976).Article 
    ADS 
    CAS 

    Google Scholar 
    Harbison, G. R. & McAlister, V. L. The filter-feeding rates and particle retention efficiencies of 3 species of Cyclosalpa (Tunicata, Thaliacea). Limnol. Oceanogr. 24, 875–892 (1979).Article 
    ADS 

    Google Scholar 
    Mullin, M. M. In situ measurement of filtering rates of the salp Thalia democratica, on phytoplankton and bacteria. J. Plankton Res. 5, 279–288 (1983).Article 

    Google Scholar 
    Deibel, D. Clearance rates of the salp Thalia democratica fed naturally occurring particles. Mar. Biol. 86, 47–54 (1985).Article 

    Google Scholar 
    Fender, C. K. et al. Prey size spectra and predator:prey ratios of 7 species of New Zealand salps. Mar. Biol. (in press).Chiswell, S. M., Bostock, H. C., Sutton, P. J. H. & Williams, M. J. M. Physical oceanography of the deep seas around New Zealand: a review. N.Z. J. Mar. Freshw. Res. 49, 286–317 (2015).Article 

    Google Scholar 
    Henschke, N. et al. Salp-falls in the Tasman Sea: a major food input to deep-sea benthos. Mar. Ecol. Prog. Ser. 491, 165–175 (2013).Article 
    ADS 

    Google Scholar 
    Childerhouse, S., Dix, B. & Gales, N. Diet of new Zealand sea lions (Phocarctos hookeri) at the Auckland islands. Wildl. Res. 28, 291–298 (2001).Article 

    Google Scholar 
    Horn, P. L., Burrell, T., Connell, A. & Dunn, M. R. A comparison of the diets of silver (Seriolella punctata) and white (Seriolella caerulea) warehou. Mar. Biol. Res. 7, 576–591 (2011).Article 

    Google Scholar 
    Horn, P. L., Forman, J. S. & Dunn, M. R. Dietary partitioning by two sympatric fish species, red cod (Pseudophycis bachus) and sea perch (Helicolenus percoides), on Chatham Rise, New Zealand. Mar. Biol. Res. 8, 624–634 (2012).Article 

    Google Scholar 
    Forman, J. S., Horn, P. L. & Stevens, D. W. Diets of deepwater Oreos (Oreosomatidae) and orange roughy Hoplostethus atlanticus. J. Fish. Biol. 88, 2275–2302 (2016).Article 
    CAS 

    Google Scholar 
    Carroll, E. L. et al. Multi-locus DNA metabarcoding of zooplankton communities and scat reveal trophic interactions of a generalist predator. Sci. Rep. 9, 1–14 (2019).Savoye, N. et al. 234Th sorption and export models in the water column: a review. Mar. Chem. 100, 234–249 (2006).Article 
    CAS 

    Google Scholar 
    Sutton, P. J. H. The Southland Current: a subantarctic current. N.Z. J. Mar. Freshw. Res. 37, 645–652 (2003).Article 

    Google Scholar 
    Foxton, P. The distribution and life history of Salpa thompsoni Foxton with observations on a related species, Salpa gerlachei Foxton. Discovery Rep. 34, 1–116 (1966).Loeb, V. J. & Santora, J. A. Population dynamics of Salpa thompsoni near the Antarctic Peninsula: growth rates and interannual variations in reproductive activity (1993–2009). Prog. Oceanogr. 96, 93–107 (2012).Article 
    ADS 

    Google Scholar 
    Pakhomov, E. A. & Hunt, B. P. V. Trans-Atlantic variability in ecology of the pelagic tunicate Salpa thompsoni near the Antarctic Polar Front. Deep-Sea Res. Part II 138, 126–140 (2017).Article 

    Google Scholar 
    Lüskow, F., Pakhomov, E. A., Stukel, M. R. & Décima, M. Biology of Salpa thompsoni at the Chatham Rise, New Zealand: demography, growth, and diel vertical migration. Mar. Biol. 167, 1–18 (2020).Pakhomov, E. A. & Froneman, P. W. Zooplankton dynamics in the eastern Atlantic sector of the Southern Ocean during the austral summer 1997/1998—Part 2: grazing impact. Deep-Sea Res. Part II 51, 2617–2631 (2004).Article 
    ADS 

    Google Scholar 
    Iversen, M. H. et al. Sinkers or floaters? Contribution from salp pellets to the export flux during a large bloom event in the Southern. Ocean. Deep-Sea Res. Part II 138, 116–125 (2017).Article 
    CAS 

    Google Scholar 
    Buesseler, K. O., Boyd, P. W., Black, E. E. & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proc. Natl Acad. Sci. USA 117, 9679 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    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).Article 

    Google Scholar 
    Hall, J., Safi, K. & Cumming, A. Role of microzooplankton grazers in the subtropical and subantarctic waters to the east of New Zealand. N.Z. J. Mar. Freshw. Res. 38, 91–101 (2004).Article 

    Google Scholar 
    Zeldis, J. R. & Décima, M. Mesozooplankton connect the microbial food web to higher trophic levels and vertical export in the New Zealand Subtropical Convergence Zone. Deep-Sea Res. Part I 155, 103146 (2020).Article 
    CAS 

    Google Scholar 
    Hall, J. A., James, M. R. & Bradford-Grieve, J. M. Structure and dynamics of the pelagic microbial food web of the Subtropical Convergence region east of New Zealand. Aquat. Micro. Ecol. 20, 95–105 (1999).Article 

    Google Scholar 
    Bradford-Grieve, J. M. et al. Pelagic ecosystem structure and functioning in the subtropical front region east of New Zealand in austral winter and spring 1993. J. Plankton Res. 21, 405–428 (1999).Article 

    Google Scholar 
    Nodder, S. & Gall, M. Pigment fluxes from the Subtropical Convergence region, east of New Zealand: relationships to planktonic community structure. N.Z. J. Mar. Freshw. Res. 32, 441–465 (1998).Article 
    CAS 

    Google Scholar 
    Nodder, S. D., Chiswell, S. M. & Northcote, L. C. Annual cycles of deep-ocean biogeochemical export fluxes in subtropical and subantarctic waters, southwest Pacific Ocean. J. Geophys. Res.: Oceans 121, 2405–2424 (2016).Article 
    ADS 
    CAS 

    Google Scholar 
    Kiko, R. et al. Biological and physical influences on marine snowfall at the equator. Nat. Geosci. 10, 852-+ (2017).Article 
    ADS 
    CAS 

    Google Scholar 
    Kelly, R. P., Shelton, A. O. & Gallego, R. Understanding PCR processes to draw meaningful conclusions from environmental DNA studies. Sci. Rep. 9, 12133 (2019).Article 
    ADS 

    Google Scholar 
    Caron, D. A., Madin, L. P. & Cole, J. J. Composition and degradation of salp fecal pellets: implications for vertical flux in oceanic environments. J. Mar. Res. 47, 829–850 (1989).Article 
    CAS 

    Google Scholar 
    Sempere, R., Yoro, S., Wambeke, F. V. & Charriere, B. Microbial decomposition of large organic particles in the northwestern Mediterranean Sea: an experimental approach. Mar. Ecol. Prog. Ser. 198, 61–72 (2000).Article 
    ADS 

    Google Scholar 
    Dell’Anno, A. & Corinaldesi, C. Degradation and turnover of extracellular DNA in marine sediments: ecological and methodological considerations. Appl. Environ. Microbiol. 70, 4384–4386 (2004).Article 
    ADS 

    Google Scholar 
    Torti, A., Lever, M. A. & Jørgensen, B. B. Origin, dynamics, and implications of extracellular DNA pools in marine sediments. Mar. Genomics 24, 185–196 (2015).Article 

    Google Scholar 
    Norris, R. Sediments of the Chatham Rise. N.Z. Dep. Sci. Ind. Res. Res. Bull. 159, 38 (1964).
    Google Scholar 
    Waite, A. M., Safi, K. A., Hall, J. A. & Nodder, S. D. Mass sedimentation of picoplankton embedded in organic aggregates. Limnol. Oceanogr. 45, 87–97 (2000).Article 
    ADS 

    Google Scholar 
    Gafar, N. A. & Schulz, K. G. A three-dimensional niche comparison of Emiliania huxleyi and Gephyrocapsa oceanica: reconciling observations with projections. Biogeosciences 15, 3541–3560 (2018).Article 
    ADS 
    CAS 

    Google Scholar 
    Eynaud, F., Giraudeau, J., Pichon, J. J. & Pudsey, C. J. Sea-surface distribution of coccolithophores, diatoms, silicoflagellates and dinoflagellates in the South Atlantic Ocean during the late austral summer 1995. Deep-Sea Res. Part I 46, 451–482 (1999).Article 

    Google Scholar 
    Hagino, K., Okada, H. & Matsuoka, H. Coccolithophore assemblages and morphotypes of Emiliania huxleyi in the boundary zone between the cold Oyashio and warm Kuroshio currents off the coast of Japan. Mar. Micropaleontol. 55, 19–47 (2005).Article 
    ADS 

    Google Scholar 
    Rhodes, L. L., Peake, B. M., Mackenzie, A. L. & Marwick, S. Coccolithophores Gephyrocapsa oceanica and Emiliana Huxleyi (Prymnesiophyceae = Haptophyceae) in New Zealand’s coastal waters: characteristics of blooms and growth in laboratory culture. N.Z. J. Mar. Freshw. Res. 29, 345–357 (1995).Article 

    Google Scholar 
    Ziveri, P., de Bernardi, B., Baumann, K.-H., Stoll, H. M. & Mortyn, P. G. Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean. Deep-Sea Res. Part II 54, 659–675 (2007).Article 
    ADS 

    Google Scholar 
    Buesseler, K. O. et al. VERTIGO (VERtical Transport In the Global Ocean): a study of particle sources and flux attenuation in the North Pacific. Deep Sea Res. II 55, 1522–1539 (2008).Article 
    ADS 

    Google Scholar 
    Billett, D. S. M., Lampitt, R. S., Rice, A. L. & Mantoura, R. F. C. Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302, 520–522 (1983).Article 
    ADS 
    CAS 

    Google Scholar 
    Martin, J. H., Fitzwater, S. E., Gordon, R. M., Hunter, C. N. & Tanner, S. J. Iron, primary production and carbon nitrogen fluxes during the JGOFS North Atlantic Bloom Experiment. Deep-Sea Res. Part II 40, 115–134 (1993).Article 
    ADS 
    CAS 

    Google Scholar 
    Buesseler, K. O. et al. The effect of marginal ice-edge dynamics on production and export in the Southern Ocean along 170 degrees W. Deep-Sea Res. Part II 50, 579–603 (2003).Article 
    ADS 
    CAS 

    Google Scholar 
    Kiko, R. et al. Zooplankton-mediated fluxes in the eastern tropical north. Atl. Front. Mar. Sci. 7, 21 (2020).
    Google Scholar 
    Kelly, T. B. et al. The importance of mesozooplankton diel vertical migration for sustaining a mesopelagic food web. Front. Mar. Sci. 6, 508 (2019).Maiti, K., Charette, M. A., Buesseler, K. O. & Kahru, M. An inverse relationship between production and export efficiency in the Southern Ocean. Geophys. Res. Lett. 40, 1557–1561 (2013).Article 
    ADS 

    Google Scholar 
    Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).Article 
    ADS 
    CAS 

    Google Scholar 
    Steinberg, D. K. et al. Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep-Sea Res. Part I 101, 54–70 (2015).Article 

    Google Scholar 
    Cabanes, D. J. E. et al. First evaluation of the role of salp fecal pellets on iron biogeochemistry. Front. Mar. Sci. 3, 10 (2017).Article 

    Google Scholar 
    Belcher, A. et al. Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone. Nat. Commun. 10, 1–8 (2019).Manno, C. et al. Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean. Nat. Commun. 11, 6051 (2020).Article 
    ADS 
    CAS 

    Google Scholar 
    Law, C. S. et al. Did dilution limit the phytoplankton response to iron addition in HNLCLSi sub-Antarctic waters during the SAGE experiment? Deep-Sea Res. Part II 58, 786–799 (2011).Article 
    ADS 
    CAS 

    Google Scholar 
    Gutiérrez‐Rodríguez, A. et al. Decoupling between phytoplankton growth and microzooplankton grazing enhances productivity in Subantarctic waters on Campbell Plateau, southeast of New Zealand. J. Geophys. Res.: Oceans 125, e2019JC015550 (2020).Sherman, J., Gorbunov, M. Y., Schofield, O. & Falkowski, P. G. Photosynthetic energy conversion efficiency in the West Antarctic Peninsula. Limnol. Oceanogr. 65, 1–14 (2020).Peterson, B. J. Aquatic primary productivity and the 14C-CO2 method: a history of the productivity problem. Annu Rev. Ecol. Syst. 11, 359–385 (1980).Article 

    Google Scholar 
    Landry, M. R. & Hassett, R. P. Estimating the grazing impact of marine microzooplankton. Mar. Biol. 67, 283–288 (1982).Article 

    Google Scholar 
    Landry, M. R., Haas, L. W. & Fagerness, V. L. Dynamics of microbial plankton communities—experiments in Kaneohe Bay, Hawaii. Mar. Ecol. Prog. Ser. 16, 127–133 (1984).Article 
    ADS 
    CAS 

    Google Scholar 
    Gutierrez-Rodriguez, A., Latasa, M., Estrada, M., Vidal, M. & Marrase, C. Carbon fluxes through major phytoplankton groups during the spring bloom and post-bloom in the Northwestern Mediterranean Sea. Deep Sea Res. Part I 57, 486–500 (2010).Article 
    CAS 

    Google Scholar 
    Gutierrez-Rodriguez, A. & Latasa, M. Pigment-based measurements of phytoplankton rates. in Phytoplankton Pigments Characterization, Chemotaxonomy and Applications in Oceanography (eds Roy, S. et al.) (Cambridge University Press, 2011) 472–495.Lorenzen, C. J. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol. Oceanogr. 12, 343–346 (1967).Article 
    ADS 
    CAS 

    Google Scholar 
    Conover, R. J., Durvasula, R., Roy, S. & Wang, R. Probable loss of chlorophyll-derived pigments during passage through the gut of zooplankton, and some of the consequences. Limnol. Oceanogr. 31, 878–887 (1986).Article 
    ADS 
    CAS 

    Google Scholar 
    Latasa, M. A simple method to increase sensitivity for RP-HPLC phytoplankton pigment analysis. Limnol. Oceanogr. Meth 12, 46–53 (2014).Article 

    Google Scholar 
    Caporaso, J. G., Paszkiewicz, K., Field, D., Knight, R. & Gilbert, J. A. The Western English Channel contains a persistent microbial seed bank. ISME J. 6, 1089–1093 (2012).Article 
    CAS 

    Google Scholar 
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581-+ (2016).Article 
    CAS 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).Article 
    CAS 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).Oksanen, J. et al. vegan: community ecology package. R package version 2.5-6. (2019).Piredda, R. et al. Diversity and temporal patterns of planktonic protist assemblages at a Mediterranean Long Term Ecological Research site. FEMS Microbiol. Ecol. 93, fiw200 (2017).Guillou, L. et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604 (2013).Article 
    CAS 

    Google Scholar 
    Pike, S. M., Buesseler, K. O., Andrews, J. & Savoye, N. Quantification of Th-234 recovery in small volume sea water samples by inductively coupled plasma-mass spectrometry. J. Radioanal. Nucl. Chem. 263, 355–360 (2005).Article 
    CAS 

    Google Scholar 
    Benitez-Nelson, C. R. et al. Testing a new small-volume technique for determining Th-234 in seawater. J. Radioanal. Nucl. Chem. 248, 795–799 (2001).Article 
    CAS 

    Google Scholar 
    Bone, Q. The Biology of Pelagic Tunicates (Oxford University Press, 1998).Foxton, P. An aid to the detailed examination of salps [Tunicata: Salpidae]. J. Mar. Biol. Assoc. UK 45, 679–681 (1965).Article 

    Google Scholar 
    Thompson, H. Pelagic Tunicates of Australia (Commonwealth Council for Scientific and Industrial Research, 1948).Iguchi, N. & Ikeda, T. Metabolism and elemental composition of aggregate and solitary forms of Salpa thompsoni (Tunicata: Thaliacea) in waters off the Antarctic Peninsula during austral summer 1999. J. Plankton Res. 26, 1025–1037 (2004).Article 
    CAS 

    Google Scholar 
    von Harbou, L. et al. Salps in the Lazarev Sea, Southern Ocean: I. feeding dynamics. Mar. Biol. 158, 2009–2026 (2011).Article 

    Google Scholar 
    Pakhomov, E. A., Dubischar, C. D., Strass, V., Brichta, M. & Bathmann, U. V. The tunicate Salpa thompsoni ecology in the Southern Ocean. I. Distribution, biomass, demography and feeding ecophysiology. Mar. Biol. 149, 609–623 (2006).Article 

    Google Scholar 
    Huntley, M. E., Sykes, P. F. & Marin, V. Biometry and trophodynamics of Salp thompsoni Foxton (Tunicata, Thaliacea) near the Antarctic peninsula in austral summer 1983–1984. Polar Biol. 10, 59–70 (1989).Article 

    Google Scholar 
    Knauer, G. A., Martin, J. H. & Bruland, K. W. Fluxes of particulate carbon, nitrogen, and phosphorus in the upper water column of the northeast Pacific. Deep Sea Res. Part I 26, 97–108 (1979).Article 
    ADS 
    CAS 

    Google Scholar 
    Karl, D. M. et al. Seasonal and interannual variability in primary production and particle flux at Station ALOHA. Deep-Sea Res. Part II 43, 539–568 (1996).Article 
    ADS 
    CAS 

    Google Scholar  More

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    Spider mites avoid caterpillar traces to prevent intraguild predation

    All the materials followed relevant institutional and national guidelines and legislation.MitesWe used a T. kanzawai population collected from trifoliate orange trees (Poncirus trifoliata [L.] Raf.) in 2018 in Kyoto, Japan, and a T. urticae population collected from chrysanthemum plants (Chrysanthemum morifolium Ramat.) in 1998 in Nara, Japan. These populations were reared on adaxial surfaces of kidney bean (Phaseolus vulgaris L.) primary leaves, which were pressed onto water-saturated cotton in Petri dishes (90 mm diameter, 14 mm depth). The water-saturated cotton served as a barrier to prevent mites from escaping. The dishes were maintained at 25 °C, 50% relative humidity, and a 16L:8D photoperiod. All experiments were conducted under these conditions. We only used mated adult females (i.e., the dispersal stage) of T. kanzawai or T. urticae mites.CaterpillarsWe used caterpillars of four lepidopteran species: Bombyx mori L., P. Xuthus, Spodoptera litura Fabricius and T. oldenlandiae. We collected eggs and larvae of T. oldenlandiae from C. japonica in 2021 in Kyoto, Japan, and reared them on C. japonica leaves until pupation. Theretra oldenlandiae shares Vitaceae host plants with T. kanzawai and T. urticae8,15. We collected eggs and larvae of P. xuthus from Ptelea trifoliata in 2021 in Kyoto, Japan, and reared them on Citrus unshiu Markov. leaves until pupation. Papilio. xuthus and T. kanzawai share P. trifoliata as a host plant in Kyoto (Kinto, personal observation).We obtained commercial populations of the B. mori Kinshu × Showa strain (Ueda-sanshu Co., Ltd, Nagano, Japan) or the w1-pnd strain. We reared B. mori larvae on an artificial diet produced at the Kyoto Institute of Technology. Although T. kanzawai use Morus alba, a food plant for the B. mori strain, the mite and the strain never encounter one another in the wild, because the B. mori strain has been domesticated for hundreds of years.We obtained a sub-cultured population of S. litura from the Kyoto Institute of Technology. We reared first to fourth instars of S. litura on an artificial diet (Insecta LFM, Nosan Insect Materials, Kanagawa, Japan), while final instars were fed P. vulgaris leaves. Because S. litura feeds on various wild and cultivated plants22,23, it may share some host plants with T. kanzawai and T. urticae, both of which also feed on many host plant species8,9,10.We reared caterpillars of T. oldenlandiae, P. xuthus, and S. litura in 900 mL transparent plastic cups and caterpillars of B. mori in transparent plastic containers (140 × 220 × 35 mm). All caterpillars were maintained under the same laboratory conditions described above.PlantsWe used several parts of P. vulgaris plants in the following experiments. This species is a preferred food for both mite species16,17 and S. litura24, but the other three caterpillar species do not feed on it (Kinto, personal observation). We thus used P. vulgaris rather than shared host plants, because some caterpillars and mites (T. urticae and P. xuthus, for example) do not share any host plant.Avoidance of caterpillar traces on leaf surfaces by spider mitesTo examine whether spider mites avoid settling on host plant surfaces bearing caterpillar traces, we conducted dual-choice tests using paired adjacent leaf squares with and without caterpillar traces. We did not use whole plants because, in practice, it was difficult to induce caterpillar traces on whole plants. We used two spider mite species (T. kanzawai and T. urticae) and four caterpillar species (T. oldenlandiae, P. xuthus, B. mori, and S. litura). We cut a 10 × 20 mm leaf piece from a fully expanded primary kidney bean leaf and then cut the piece into two equal squares (10 × 10 mm). To introduce caterpillar traces to one square, we arranged them on a separate piece of paper towel on water-saturated cotton. This procedure was necessary because the caterpillars used were larger than individual leaf squares. Then we placed a fourth or final instar caterpillar on the squares and induced the caterpillar to walk across every leaf square three times (Fig. 1a). We carefully removed all caterpillar-produced silk threads from the squares. Within 30 min, we arranged the square (trace +) to touch against the other square (trace −) on water-saturated cotton in a Petri dish. Subsequently, a 2- to 4-day-old mated adult female of T. kanzawai or T. urticae was introduced onto a pointed piece of Parafilm in contact with both leaf edges using a fine brush (Fig. 1a). We recorded the leaf square onto which the mite had settled at 2 h after its introduction, as preliminary observations confirmed that all females would settle on a particular leaf within that period. Each female mite and pair of leaf squares were used only once. All tests described below were conducted between 13:00 and 17:00 h, when adult female spider mites actively disperse by walking. There were 14 replicates using traces of T. oldenlandiae, 48 of P. xuthus, 20 of B. mori, and 26 of S. litura for T. kanzawai, as well as 18, 32, 16, and 47, respectively, for T. urticae. Data were subjected to two-tailed binomial tests with the common null hypothesis that a spider mite would settle on the two squares with equal probability (i.e., 0.5).Figure 1(a) Procedure used to observe avoidance of caterpillar traces by spider mites. (b) Experimental setup used to observe avoidance of B. mori traces on plant stems by T. kanzawai. (c) Experimental setup used to observe avoidance of B. mori trace extracts by T. kanzawai.Full size imageDuration of B. mori trace avoidance by T. kanzawai
    To examine whether the effects of caterpillar traces on spider mite avoidance decline over time, we used T. kanzawai mites and B. mori caterpillars. We used B. mori because populations can be easily maintained over many generations. We prepared bean leaf squares with B. mori traces in the same manner descried above and preserved the traced square on water-saturated cotton for 0 h (n = 30), 24 h (n = 29), 48 h (n = 28), or 72 h (n = 28). Then we arranged the square (trace +) to lie in close proximity to the control square (trace −) that had been preserved for the same periods of time. Then we compared the avoidance response of T. kanzawai females in the same manner described above.Avoidance of B. mori traces on plant stems by T. kanzawai
    To examine whether T. kanzawai females avoid walking along plant stems bearing caterpillar traces, we used Y-shaped kidney bean stems (Fig. 1b). We cut symmetric bean plants ca. 15 days after sowing from their base and inserted them perpendicularly into a 5 mL glass bottle filled with water and wet cotton. To induce caterpillar traces on one branch of the stem, we allowed a silkworm to crawl from the branching point to the far end of one branch three times for each stem (n = 20). Then we introduced a T. kanzawai adult female at a release point 35 mm below the branch point (Fig. 1b). We recorded the branch along which the female walked to the far end. Each female mite and each Y-shaped stem were used only once. The numbers of females were compared using binomial tests in the same manner described above.Avoidance of B. mori trace extracts by T. kanzawai
    To extract chemical traces of caterpillar, we introduced 10 third instar B. mori to a glass Petri dish (120 mm diameter, 60 mm depth). After 1 h, we removed all caterpillars and washed the inside bottom of the dish with 1.0 mL acetone. We replicated the procedure twice using different individuals to combine all extracts and to acquire enough extract for the following experiment.To examine avoidance of B. mori trace extracts by T. kanzawai females, we conducted dual-choice experiments using T-shaped pathways of filter paper (35 × 35 mm; width, 2 mm; Fig. 1c). Using disposable micropipettes (Drummond Scientific Co., PA, USA), 1.75 caterpillar equivalents (i.e., 60 µL) of acetone extract were applied to an alternately selected branch (17.5 mm long) of each pathway (i.e., 0.10 caterpillar equivalent/mm), with control acetone applied to the other branch. We applied each solution dropwise at the junction point to minimize mixing. After evaporating the solvent from those pathways, we perpendicularly suspended them (Fig. 1c) and introduced an adult female mite at 2 days post-maturation onto the bottom of each pathway using a fine brush and recorded the branch along which the female first walked to the far end. Each female mite and each T-shaped filter paper were used only once, with 19 replicates. Each female mite made a choice within 10 min. The avoidance response of T. kanzawai was analysed in the same manner described above.Indirect effects of B. mori traces on T. kanzawai via plantsTo determine whether B. mori traces on plants indirectly affect the performance of T. kanzawai on plants, we introduced 70–80 randomly selected quiescent female deutonymphs of T. kanzawai onto kidney bean leaf disks. Immediately after synchronized adult emergence, we introduced the same number of adult males to allow mating; the detailed procedure is described elsewhere25. After 24 h, we transferred the females singly onto 10 × 10 mm bean leaf squares with or without B. mori traces prepared as described above. Because the number of eggs laid within a certain period is considered the most sensitive performance index of spider mite females26,27, any plant-mediated indirect interaction, such as defence induction in response to caterpillar traces, should result in lower egg numbers laid by the test females. We counted the eggs laid on the leaf squares 24 h after their introduction. One female that laid no eggs during the 24 h period (n = 1, trace +) was excluded from the analysis. We obtained 33 and 36 replicates for the trail+ and trail– conditions, respectively. We compared the numbers of eggs laid on leaves with and without B. mori traces using a generalized linear model with a Poisson error distribution using the SAS 9.22 software (SAS Institute Inc., Cary, NC, USA).EthicsThis article does not contain any studies with human participants or animals. More

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    Tamarixia radiata global distribution to current and future climate using the climate change experiment (CLIMEX) model

    Arunrat, N., Sereenonchai, S., Chaowiwat, W. & Wang, C. Climate change impact on major crop yield and water footprint under CMIP6 climate projections in repeated drought and flood areas in Thailand. Sci. Total Environ. 807, 150741 (2022).ADS 
    CAS 

    Google Scholar 
    Chandio, A. A., Shah, M. I., Sethi, N. & Mushtaq, Z. Assessing the effect of climate change and financial development on agricultural production in ASEAN-4: the role of renewable energy, institutional quality, and human capital as moderators. Environ. Sci. Pollut. Res. 29, 13211–13225 (2022).
    Google Scholar 
    Masood, N., Akram, R., Fatima, M., Mubeen, M., Hussain, S., Shakeel, M., Khan, N., Adnan, M., Wahid, A., Shah, A. N. and Ihsan, M. Z. (2022) Insect pest management under climate change. In Building climate resilience in agriculture. Springer, ChamOzdemir, D. The impact of climate change on agricultural productivity in Asian countries: A heterogeneous panel data approach. Environ. Sci. Pollut. Res. 29, 8205–8217 (2022).
    Google Scholar 
    Aidoo, O. F. et al. Climate-induced range shifts of invasive species (Diaphorina citri Kuwayama). Pest Manag. Sci. 78, 2534–2549 (2022).CAS 

    Google Scholar 
    Hebbar, K. B. et al. Predicting the Potential Suitable Climate for Coconut (Cocos nucifera L.) Cultivation in India under Climate Change Scenarios Using the MaxEnt Model. Plants. 11, 731 (2022).
    Google Scholar 
    Martín-Vélez, V. & Abellán, P. Effects of climate change on the distribution of threatened invertebrates in a Mediterranean hotspot. Insect Conserv. Divers. 15, 370–379 (2022).
    Google Scholar 
    Williams, J. J., Freeman, R., Spooner, F. & Newbold, T. Vertebrate population trends are influenced by interactions between land use, climatic position, habitat loss and climate change. Glob. Chang. Biol. 28, 797–815 (2022).CAS 

    Google Scholar 
    Aidoo, O. F. et al. Lethal yellowing disease: insights from predicting potential distribution under different climate change scenarios. J. Plant Dis. Prot. 128, 1313–1325 (2021).
    Google Scholar 
    Sofaer, H. R. et al. Development and delivery of species distribution models to inform decision-making. Bioscience 69, 544–557 (2019).
    Google Scholar 
    Mead FW, The Asiatic citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae). Florida Department of Agriculture Conservation Service, Division of Plant Industry Entomological Circular No. 180.Bové, J. M. Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Plant Pathol. J. 1, 7–37 (2006).
    Google Scholar 
    Li, S., Wu, F., Duan, Y., Singerman, A. & Guan, Z. Citrus greening: Management strategies and their economic impact. HortScience 55, 604–612 (2020).
    Google Scholar 
    Jia, H. et al. Genome editing of the disease susceptibility gene Cs LOB 1 in citrus confers resistance to citrus canker. Plant Biotechnol. J. 15, 817–823 (2017).CAS 

    Google Scholar 
    Ehsani, R., Dewdney, M. & Johnson, E. Controlling HLB with thermotherapy: What have we learned so far?. Citrus Ind. News 9, 26–28 (2016).
    Google Scholar 
    Spreen, T. H., Baldwin, J. P. & Futch, S. H. An economic assessment of the impact of Huanglongbing on citrus tree plantings in Florida. J. Hortic. Sci. 49, 1052–1055 (2014).
    Google Scholar 
    Djeddour, D., Pratt, C., Constantine, K., Rwomushana, I. and Day, R., (2021) The Asian citrus greening disease (Huanglongbing). Evidence note on invasiveness and potential economic impacts for East Africa. CABI Working Paper, 24, 94Hu, J., Jiang, J. & Wang, N. Control of citrus Huanglongbing via trunk injection of plant defense activators and antibiotics. Phytopathology 108, 186–195 (2018).CAS 

    Google Scholar 
    Fan, G. C. et al. Evaluation of thermotherapy against Huanglongbing (citrus greening) in the greenhouse. J. Integr. Agric. 15, 111–119 (2016).
    Google Scholar 
    Nguyen, V. A., Bartels, D. & Gilligan, C. Modelling the spread and mitigation of an emerging vector-borne pathogen: citrus greening in the US. Biorxiv https://doi.org/10.1101/2022.05.04.490566 (2022).Article 

    Google Scholar 
    Milosavljević, I. et al. Post-release evaluation of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) and Tamarixia radiata (Hymenoptera: Eulophidae) for biological control of Diaphorina citri (Hemiptera: Liviidae) in Urban California, USA. Agronomy 12, 583 (2022).
    Google Scholar 
    Maluta, N., Castro, T. & Lopes, J. R. S. Entomopathogenic fungus disrupts the phloem-probing behavior of Diaphorina citri and may be an important biological control tool in citrus. Sci. Rep. 12, 1–10 (2022).
    Google Scholar 
    Hall, D. G., Richardson, M. L., Ammar, E. D. & Halbert, S. E. Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease. Entomol. Exp. Appl. 146, 207–223 (2013).
    Google Scholar 
    Vázquez-García, M. et al. Insecticide resistance in adult Diaphorina citri Kuwayama1 from lime orchards in central west Mexico. Southwest. Entomol. 38, 579–596 (2013).
    Google Scholar 
    Naeem, A., Freed, S., Jin, F. L., Akmal, M. & Mehmood, M. Monitoring of insecticide resistance in Diaphorina citri Kuwayama (Hemiptera: Psyllidae) from citrus groves of Punjab Pakistan. Crop Prot. 86, 62–68 (2016).CAS 

    Google Scholar 
    Hulme, P. E. et al. Grasping at the routes of biological invasions: A framework for integrating pathways into policy. J. Appl. Ecol. 45, 403–414 (2008).
    Google Scholar 
    Oke, A. O., Oladigbolu, A. A., Kunta, M., Alabi, O. J. & Sétamou, M. First report of the occurrence of Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae), an invasive species in Nigeria. West Africa. Sci. Rep. 10, 1–8 (2020).
    Google Scholar 
    Tang, Y.Q. (1990) On the parasite complex of Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Asian-Pacific and other areas. In proceedings 4th international conference on citrus rehabilitation, Chiang Mai, Thailand. 4: 240 245Chien, C. C., Chiu, S. C. & Ku, S. C. Biological control of Diaphorina citri in Taiwan. Fruits 44, 401–407 (1989).
    Google Scholar 
    Hoddle, M. S. Foreign exploration for natural enemies of Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae), in the Punjab of Pakistan for use in a classical biological control program in California USA. Pakistan Entomol. 34, 1–5 (2012).
    Google Scholar 
    Étienne, J., Quilici, S., Marival, D., Franck, A. & Gonzalez Fernandez, C. Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eulophidae). Fruits 56, 307–315 (2001).
    Google Scholar 
    Qureshi, J. A., Rogers, M. E., Hall, D. G. & Stansly, P. A. Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. J. Econ. Entomol. 102, 247–256 (2009).
    Google Scholar 
    Chen, X., Triana, M. & Stansly, P. A. Optimizing production of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of the citrus greening disease vector Diaphorina citri (Hemiptera: Psylloidea). Biol. Control. 105, 13–18. https://doi.org/10.1016/j.biocontrol.2016.10.010 (2017).Article 

    Google Scholar 
    Kistner, E. J., Amrich, R., Castillo, M., Strode, V. & Hoddle, M. S. Phenology of Asian citrus psyllid (Hemiptera: Liviidae), with special reference to biological control by Tamarixia radiata, in the residential landscape of southern California. J. Econ. Entomol. 109, 1047–1057. https://doi.org/10.1093/jee/tow021 (2016).Article 

    Google Scholar 
    Ramos Aguila, L. C. et al. Temperature-dependent biological control effectiveness of Tamarixia radiata (Hymenoptera: Eulophidea) under laboratory conditions. J. Econ. Entomol. 114, 2009–2017 (2021).
    Google Scholar 
    Ramos Aguila, L. C. et al. Temperature-dependent demography and population projection of Tamarixia radiata (Hymenoptera: Eulophidea) reared on Diaphorina citri (Hemiptera: Liviidae). J. Econ. Entomol. 113, 55–63 (2020).
    Google Scholar 
    Ashraf, H. J. et al. Comparative microbiome analysis of Diaphorina citri and its associated parasitoids Tamarixia radiata and Diaphorencyrtus aligarhensis reveals Wolbachia as a dominant endosymbiont. Environ. Microbiol. 24, 1638–1652 (2022).CAS 

    Google Scholar 
    Chow, A. & Sétamou, M. Parasitism of Diaphorina citri (Hemiptera: Liviidae) by Tamarixia radiata (Hymenoptera: Eulophidae) on residential citrus in Texas: Importance of colony size and instar composition. Biol. Control 165, 104796 (2022).
    Google Scholar 
    Ajene, I. J. et al. Habitat suitability and distribution potential of Liberibacter species (“Candidatus Liberibacter asiaticus” and “Candidatus Liberibacter africanus”) associated with citrus greening disease. Environ. Microbiol. 26, 575–588 (2020).
    Google Scholar 
    Shabani, F., Kumar, L. & Ahmadi, M. A comparison of absolute performance of different correlative and mechanistic species distribution models in an independent area. Ecol. Evol. 6, 5973–5986 (2016).
    Google Scholar 
    Kearney, M. & Porter, W. Mechanistic niche modelling: Combining physiological and spatial data to predict species’ ranges. Ecol 12, 334–350 (2009).
    Google Scholar 
    Byeon, D. H., Jung, S. & Lee, W. H. Review of CLIMEX and MaxEnt for studying species distribution in South Korea. J. Asia-Pac. Biodivers. 1, 325–333 (2018).
    Google Scholar 
    Kriticos, D. J., Yonow, T. & McFadyen, R. E. The potential distribution of Chromolaena odorata (Siam weed) in relation to climate. Weed Res 45, 246–254 (2005).
    Google Scholar 
    Wharton, T. N. & Kriticos, D. J. The fundamental and realized niche of the Monterey pine aphid, Essigella californica (Essig) (Hemiptera: Aphididae): implications for managing softwood plantations in Australia. Divers. Distrib. 10, 253–262 (2004).
    Google Scholar 
    Sutherst, R., Maywald, G. and Kriticos, D., CLIMEX version 3: user’s guide. (2007).Ramirez-Cabral, N. Y., Kumar, L. & Shabani, F. Global alterations in areas of suitability for maize production from climate change and using a mechanistic species distribution model (CLIMEX). Sci. Rep. 7, 1–3 (2017).CAS 

    Google Scholar 
    McCalla, K. A., Keçeci, M., Milosavljević, I., Ratkowsky, D. A. & Hoddle, M. S. The influence of temperature variation on life history parameters and thermal performance curves of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of the Asian citrus psyllid (Hemiptera: Liviidae). J. Econ. Entomol. 112, 1560–1574 (2019).
    Google Scholar 
    Gonzalez-Cabrera, J., Moreno-Carrillo, G., Sanchez-Gonzalez, J. A. & Bernal, H. C. Natural and augmented parasitism of tamarixia radiata (Hymenoptera Eulophidae) in Urban Areas of western Mexico. Entomol. Sci. 53, 486–492. https://doi.org/10.18474/JES17-112.1 (2018).Article 

    Google Scholar 
    Chavez, Y. et al. Tamarixia radiata (Waterston) and Cheilomenes sexmaculata (Fabricius) as biological control agents of Diaphorina citri Kuwayama in Ecuador. Chil. J. Agric. Res. 77, 180–184. https://doi.org/10.4067/S0718-58392017000200180 (2017).Article 

    Google Scholar 
    Flores, D. & Ciomperlik, M. Biological control using the ectoparasitoid, Tamarixia radiata, against the Asian citrus psyllid, Diaphorina citri, in the lower Rio Grande valley of Texas. Southwest. Entomol. 42, 49–59. https://doi.org/10.3958/059.042.0105 (2017).Article 

    Google Scholar 
    Parra, J. R., Alves, G. R., Diniz, A. J. & Vieira, J. M. Tamarixia radiata (Hymenoptera: Eulophidae) × Diaphorina citri (Hemiptera: Liviidae): Mass rearing and potential use of the parasitoid in Brazil. J. Integr. Pest. Manag. https://doi.org/10.1093/jipm/pmw003 (2016).Article 

    Google Scholar 
    Diniz, A. J. F., Otimização da criação de Diaphorina citri Kuwayama, 1908 (Hemiptera: Liviidae) e de Tamarixia radiata (Waterston, 1922) (Hymenoptera: Eulophidae), visando a produção em larga escala do parasitoide e avalliação do seu estabelecimento em campo. Tese (Doutorado em Entomologia)—Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, São Paulo. (2013)Hoddle, M. S. & Pandey, R. Host range testing of Tamarixia radiata (Hymenoptera: Eulophidae) sourced from the Punjab of Pakistan for classical biological control of Diaphorina citri (Hemiptera: Liviidae: Euphyllurinae: Diaphorinini) in California. J. Econ. Entomol. 107, 125–136. https://doi.org/10.1603/EC13318 (2014).Article 

    Google Scholar 
    Gómez-Torres, M. L., Nava, D. E. & Parra, J. R. Thermal hygrometric requirements for the rearing and release of Tamarixia radiata (Waterston) (Hymenoptera, Eulophidae). Rev. Bras. Entomol. 58, 291–295. https://doi.org/10.1590/S0085-56262014000300011 (2014).Article 

    Google Scholar 
    Gómez-Torres, M. L., Nava, D. E. & Parra, J. R. Life table of Tamarixia radiata (Hymenoptera: Eulophidae) on Diaphorina citri (Hemiptera: Psyllidae) at different temperatures. J. Econ. Entomol. 105, 338–343 (2012).
    Google Scholar 
    Chong, J. H., Roda, A. L. & Mannion, C. M. Density and natural enemies of the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae), in the residential landscape of Southern Florida. J. Agric. Urban Entomol. 27, 33–49. https://doi.org/10.3954/11-05.1 (2010).Article 

    Google Scholar 
    Pluke, R. W., Qureshi, J. A. & Stansly, P. A. Citrus flushing patterns, Diaphorina citri (Hemiptera: Psyllidae) populations and parasitism by Tamarixia radiata (Hymenoptera: Eulophidae) in Puerto Rico. Florida Entomol. 91, 36–42 (2008).
    Google Scholar 
    Ashraf, H. J. et al. Genetic diversity of Tamarixia radiata populations and their associated endosymbiont Wolbachia species from China. Agronomy 11, 2018 (2021).CAS 

    Google Scholar 
    Jung, J. M., Lee, W. H. & Jung, S. Insect distribution in response to climate change based on a model: Review of function and use of CLIMEX. Entomol. Res. 46, 223–235 (2016).
    Google Scholar 
    Kriticos, D. J. et al. CLIMEX Version 4, 184p (2015).
    Google Scholar 
    Gomez-Marco, F., Gebiola, M., Baker, B. G., Stouthamer, R. & Simmons, G. S. Impact of the temperature on the phenology of Diaphorina citri (Hemiptera: Liviidae) and on the establishment of Tamarixia radiata (Hymenoptera: Eulophidae) in urban areas in the lower Colorado Desert in Arizona. Environ. Entomol. 48, 514–523 (2019).
    Google Scholar 
    Vieira, J. M. Biologia em temperaturas alternantes e exigências térmicas de Diaphorina citri Kuwayama, 1908 (Hemiptera: Liviidae) e Tamarixia radiata (Waterston, 1922) (Hymenoptera: Eulophidae) visando ao seu zoneamento em regiões citrícolas do estado (Doctoral dissertation, Universidade de São Paulo).Castillo, J., Jacas, J. A., Peña, J. E., Ulmer, B. J. & Hall, D. G. Effect of temperature on life history of Quadrastichus haitiensis (Hymenoptera: Eulophidae), an endoparasitoid of Diaprepes abbreviatus (Coleoptera: Curculionidae). Biol. Control. 36, 189–196 (2006).
    Google Scholar 
    McFarland, C. D. & Hoy, M. A. Survival of Diaphorina citri (Homoptera: Psyllidae), and its two parasitoids, Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), under different relative humidities and temperature regimes. Fla. Entomol. 84, 227–233 (2001).
    Google Scholar 
    Fauvergue, X. & Quilici, S. Etude de certains parametres de la biologie de Tamarixia radiata (Waterston, 1992)(Hymenoptera: Eulophidae), ectoparasitoide primaire de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) vecteur du greening des agrumes. Paris Fruits 46, 179–179 (1991).
    Google Scholar 
    Araújo, F. H. et al. Modelling climate suitability for Striga asiatica, a potential invasive weed of cereal crops. Crop Prot. 1(160), 106050 (2022).
    Google Scholar 
    Silva, D. A. & RS, Kumar L, Shabani F and Picanço MC,. Potential risk levels of invasive Neoleucinodes elegantalis (small tomato borer) in areas optimal for open-field Solanum lycopersicum (tomato) cultivation in the present and under predicted climate change. Pest Manag. Sci 73, 616–627 (2017).
    Google Scholar 
    Kumar, S., Neven, L. G. & Yee, W. L. Evaluating correlative and mechanistic niche models for assessing the risk of pest establishment. Ecosphere 5, 1–23. https://doi.org/10.1890/ES14-00050.1 (2014).Article 
    CAS 

    Google Scholar 
    Kriticos, D. J. et al. CliMond: global high-resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol. Evol. 1, 53–64 (2012).
    Google Scholar 
    Santana Júnior PA, Worldwide spatial distribution of Tuta absoluta (Lepidoptera: Gelechiidae) and its natural enemies under current and future climatic change conditions through modelling. 136 f 2019 (Tese (Doutorado em Fitotecnia) – Universidade Federal de Viçosa, 2019).
    Google Scholar 
    Kriticos, D. J., Maywald, G. F., Yonow, T., Zurcher, E. J., Herrmann, N. I. and Sutherst, R. W., CLIMEX Version 4: Exploring the effects of climate on plants, animals and diseases. CSIRO, Canberra.156, (2015)Ramos Aguila, L. C. et al. Temperature-dependent demography and population projection of Tamarixia radiata (Hymenoptera: Eulophidea) reared on Diaphorina citri (Hemiptera: Liviidae). J. Econ. Entomol. 113, 55–63 (2019).
    Google Scholar 
    Oliveira, R. C., Modelagem de nicho ecológico para Helicoverpa punctigera (Wallengren, 1860) (Lepidoptera: Noctuidae) no mundo: Potencial invasão e riscos diante das mudanças climáticas. (2021). http://www.repositorio.ufc.br/handle/riufc/61961Bazzocchi, G. G., Lanzoni, A., Burgio, G. & Fiacconi, M. R. Effects of temperature and host on the pre-imaginal development of the parasitoid Diglyphus isaea (Hymenoptera: Eulophidae). Biol. Control 26, 74–82 (2003).
    Google Scholar 
    Hondo, T., Koike, A. & Sugimoto, T. Comparison of thermal tolerance of seven native species of parasitoids (Hymenoptera: Eulophidae) as biological control agents against Liriomyza trifolii (Diptera: Agromyzidae) in Japan. Appl. Entomol. Zool. 41, 73–82 (2006).
    Google Scholar 
    Duale, A. Effect of temperature and relative humidity on the biology of the stem borer parasitoid Pediobius furvus (Gahan) (Hymenoptera: Eulophidae) for the management of stem borers. Environ. Entomol. 34, 1–5 (2005).
    Google Scholar 
    Ashraf, H. J. et al. Comparative transcriptome analysis of Tamarixia radiata (Hymenoptera: Eulophidae) reveals differentially expressed genes upon heat shock. Comp. Biochem. Physiol. D: Genom. Proteom. 41, 100940 (2022).CAS 

    Google Scholar 
    van Doan, C. et al. Natural enemies of herbivores maintain their biological control potential under short-term exposure to future CO2, temperature, and precipitation patterns. Ecol. Evol. 11, 4182–4192 (2021).
    Google Scholar 
    Thomson, L. J., Macfadyen, S. & Hoffmann, A. A. Predicting the effects of climate change on natural enemies of agricultural pests. Biol. Control. 52, 296–306 (2010).
    Google Scholar 
    Rosenblatt, A. E. & Schmitz, O. J. Climate change, nutrition, and bottom-up and top-down food web processes. Trends Ecol. Evol. 31, 965–975 (2016).
    Google Scholar 
    Aidoo, O. F. et al. A machine learning algorithm-based approach (MaxEnt) for predicting invasive potential of Trioza erytreae on a global scale. Ecol. Inform. 71, 101792 (2022).
    Google Scholar 
    Aidoo, O. F. et al. The Impact of Climate Change on Potential Invasion Risk of Oryctes monoceros Worldwide. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2022.895906 (2022).Article 

    Google Scholar 
    Hao, M. et al. Global potential distribution of Oryctes rhinoceros, as predicted by Boosted Regression Tree model. Glob. Ecol. Conserv. 1(37), e02175 (2022).
    Google Scholar 
    Aidoo, O. F. et al. Model-based prediction of the potential geographical distribution of the invasive coconut mite, Aceria guerreronis Keifer (Acari: Eriophyidae) based on MaxEnt. Agric. For. Entomol. 24, 390–404 (2022).
    Google Scholar  More

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    Fieldwork: how to gain access to research participants

    Anna Lena Bercht interviewed fishers in Lofoten, Norway, to assess how climate change was affecting their livelihoods.Credit: Anna Lena Bercht

    I remember February 2011, when, in the Chinese megacity of Guangzhou, an older man finally overcame his scepticism about being interviewed and invited me to sit down next to him on a stone bench under a shady tree. I held my notebook on my lap, and we sat on either side of a translator and talked about his life and world for more than two hours. It was one of the most informative and revealing interviews that I had done during my fieldwork in the city.
    Making it in the megacity
    One of the most fundamental challenges in qualitative fieldwork is gaining access to research participants. This is often time-consuming and labour-intensive, particularly when the topic requires in-depth methods and addresses a sensitive subject.Advice that goes beyond the usual recommendations of establishing relationships with gatekeepers, ensuring anonymity for interviewees and relying on the snowball sampling technique (in which one research participant suggests further ones) is rare. In this light, I’m happy to share some simple, but often neglected, examples from my qualitative fieldwork in the lively Guangzhou (where I worked for 12 months)1 and on the remote, Arctic island chain of Lofoten, Norway (done over 4 months)2, that might offer some inspiration and encouragement.I have a background in human geography, and did my PhD on experiences of stress, coping and resilience among the Chinese population of Guangzhou in the face of the city’s rapid urbanization. I travelled there five times to help to establish research cooperation with Chinese scholars, make field observations, select a case-study site and interview locals. I, together with other PhD students, stayed in a typical Chinese high-rise apartment in a neighbourhood that wasn’t a common choice for expatriates. Living side-by-side with the locals gave us a perfect opportunity to experience genuine everyday life and Chinese culture.My first postdoctoral project after my PhD brought me to Lofoten, where I looked at psychological barriers to climate adaptation in small-scale coastal fisheries. I went to Lofoten twice. On my first visit, I travelled across the whole archipelago by bus for one month to get a profound overview of the fishing villages and local living conditions, and to conduct first interviews. During my second visit, I stayed for a total of three months in rental locations near fishing harbours, and conducted more extensive interviews.In both China and Norway, I used in-depth interviews to learn about the challenges that people face. I asked people about unemployment, about the possibility of being forced to move elsewhere and about how climate change might affect their livelihoods. This required a sensitive and thoughtful approach to ‘getting invited’ into people’s lives. In Guangzhou, German- and English-speaking Chinese students assisted me as translators (and interpreters, when needed). On Lofoten, I conducted the interviews myself in English.There are two ways to access research participants: physical access, which refers to the ability of the researcher to get in direct face-to-face contact with people, and mental access. Successful mental access means that interlocutors open up about why they think, feel and behave as they do. Physical access is a necessary condition for mental access; however, in my experience, both are equally valuable.

    Chinese interviewees in Guangzou shared their feelings about the rapid urbanization of their city.Credit: Anna Lena Bercht

    Compared with Lofoten, it took longer to get physical access to local inhabitants in China. Presumably, this was because of the language barrier and reliance on translators, as well as cultural differences. Trust is considered a central tenet in Chinese relationships, and time and effort are needed to let it grow. During my time in Guangzhou, I occasionally benefited from being a foreigner: people were touched that someone from abroad showed genuine interest in their well-being. In Lofoten, fishers appreciated talking to a social scientist instead of a natural scientist who would have mainly asked questions about fishing quotas and catch volume.My advice for other social scientists hoping to gain access to research participants falls into those two categories.How to get good physical accessUse local public transport. Using local public transport creates many unexpected opportunities to bump into people, get into conversations and gain relevant information. For example, while waiting at a bus stop in Lofoten, I came across an art-gallery owner from a fishing village. He wondered why I was travelling out of the peak tourism season. I ended up with an invitation to his gallery, where he introduced me to two retired fishers whom he had also invited. Without the gallerist and his proactive networking, I probably would not have been given the chance to interview these two very informative and engaging fishers.In a metro station in Guangzhou, a toddler kept staring at me and tried to touch my light hair. This small interaction led me to chat to the toddler’s father, who recommended that I talk to a local teacher to learn more about the area’s history. His advice opened up important insights into urban-restructuring processes that I would have missed otherwise.
    Nine ‘brain food’ tips for researchers
    Use local media. In Norway, a journalist was at the harbour to get first-hand information on the year’s cod catch, when he saw me interviewing fishers. He became curious and eager to learn more about my work. In the end, he wrote an article about my research, which was published a few days later across Lofoten. His article was a door-opener for me.People recognized me from my photo in the article and contacted me to tell me about their lives and the cod fisheries. They also invited me on their vessels and put me in touch with other key informants.Change your workplace. During fieldwork, a workplace is often needed for interview transcription, literature research and interim data analysis. Moving the workplace outside wherever you are staying during a field trip allows you to immerse yourself in the daily lives of local people and interact with them more easily. For me, such agile ‘mini-office’ locations were cafes, public libraries and picnic tables. In this way, I was able to recruit interview partners on the spot.How to create deeper mental accessWear appropriate outfits. First impressions count, always. Researchers are judged not only on what they say and how they say it, but also on how they look. Certain clothes, such as those with a political slogan or religious symbol, have certain meanings and connotations. Depending on the context and whom you talk to, your appearance could promote or impede making connections and building rapport. For instance, whereas my practical ‘outdoorsy’ get-dirty outfit was appropriate for interviews on fishing vessels, a modest appearance (non-branded clothes and a simple style) was useful in rural areas of Guangzhou.Show respect. Just like in any other relationship, respect and humility play a crucial part in building a trustworthy interviewer–interviewee relationship. Showing respect can be subtly embedded in conversations in many ways, including in the content of questions and the manner in which they are asked. When interviewees started to close down when asked about painful issues, such as underemployment or loss of identity, I upheld their privacy, comfort and security by not probing when given an evasive answer. Instead, I changed the interview focus and, when appropriate, cautiously reapproached the sensitive issue by using interview techniques such as roleplaying. Interviewees were asked to put themselves in the position of someone else, such as a spatial planner or politician, and assess the issue at hand from this perspective. Taking such an imaginary role can help to make the interviewees feel more secure and face pain more openly.Be humble. Having a modest view of yourself is essential to communicate at eye level with people. As a scientist, you can easily fall into the trap of thinking that your thoughts and concepts are somehow more valuable because you are well-educated and established. However, you are the one asking questions — and the interviewees, whether they are fishers, farmers or homeless people, often know more about many things than you do. Being aware of this is an expression of humility. I let the interviewees know that they were the local experts and I was the foreign learner.Use small talk. Small talk — including non-verbal communication, such as smiling, or connective gestures, for example handing out a handkerchief or offering some tea — has an essential bonding function. Talking about ‘safe’ topics can help the interviewee to overcome the feelings of otherness, newness and discomfort that can emerge in an interview, and fosters social cohesiveness. This can help to counteract the asymmetrical power relationship between the researcher (who asks) and the researched (who answers). For example, before substantive questioning, I created shared experiences by talking about last night’s storm or the world cod-fishing championship, which takes place every year in Lofoten. This took the relationship to a greater level of intimacy and togetherness — which small talk after finishing the interview can strengthen. I remember joking about my stamina for eating properly with chopsticks to one interviewee.Use self-disclosure. Revealing selected information about yourself and sharing your own thoughts with interlocutors can help to create and reaffirm a sphere of confidentiality and trust. Fishers in Norway would, for instance, often ask “What interested you in Lofoten coastal fisheries?” or “Why do you ask me and not the scientists from Tromsø University?” I answered such questions honestly, which assisted in creating a more balanced relationship, encouraging the interviewees to address sensitive subjects more openly and readily.Change interview sites. In several interviews, I found that the answers given tended to depend on where the interview was held and which identity that site evoked for the interviewee. For example, a fisher did not talk about climate-change concerns on his fishing vessel (any concern was masked by his existential fear of losing his livelihood as a coastal fisher), but he later that day freely discussed his worries in his home. Changing the interview site can be a helpful technique to access hidden thoughts and feelings.Above all, be realistic. You will probably make mistakes; I regretted not dressing warmly enough on a fishing vessel in Arctic weather. Locals will find you amusing, weird or impolite. They will keep out of your way, and you will never know why. And they will terminate interviews prematurely with no excuse. And that’s all right. In the end, fieldwork is a combination of planning, resources, time, skills, hard work, commitment, headache, joy — and luck. Learn from your mistakes, and accept the things you cannot change. More

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    Urban agriculture in walkable neighborhoods bore fruit for health and food system resilience during the COVID-19 pandemic

    During the COVID-19 pandemic, behavioral restrictions were imposed, after which various health problems were reported in many countries45,46. The pandemic has also increased food insecurity worldwide; consequently, panic buying has been observed in many countries, including Japan47. However, even in such situations, we found that diversity in local food access, ranging from self-cultivation to direct-to-consumer sales, was significantly associated with health and food security variables. Specifically, our results revealed the following five key discussion points.Urban agriculture in walkable neighborhoods bore fruit for health and food system resilience. However, the magnitude of its contribution differed depending on the type of urban agricultureThe results of this study showed that those who grew food by themselves at allotment farms and home gardens had significantly better subjective well-being and physical activity levels than those who did not. This result is in line with previous studies conducted during times free from the impact of infectious disease pandemics38,39,40. The use of direct sales was not related to subjective well-being but was significantly associated with physical activity. The reason might be that farm stand users tend to live in areas with farmland and travel to purchase fruits and vegetables at farm stands on foot or by bicycle. This result is consistent with that of a previous study demonstrating that the food environment in neighborhoods is an important component in promoting physical activity17.Our results also showed that those who grew food by themselves at allotment farms and those who purchased local foods at farm stands were significantly less anxious about the availability of fresh food both during the state of emergency and in the future than their counterparts. In contrast, home garden users showed significant differences only for the state of emergency. This result might be due to the differences in the size and yield of cultivation at allotment farms and home gardens. One lot in allotment farms in Tokyo can produce as much as or more than the average annual vegetable consumption per household in Japan48. However, home gardens are generally smaller and produce limited fresh foods for consumption, which may have influenced food security concerns.As in other countries, Japan imports much food from overseas and is deeply integrated into the large-scale global food system. However, as shown in this study, urban agriculture in Japanese suburbs forms small-scale, decentralized, and community-based local food systems. This multilayered food system can complement the disruptions and shortages of the global system when various problems occur for climatic, sociopolitical, or other reasons, such as pandemics. In fact, our empirical evidence suggests that urban agriculture in walkable neighborhoods, particularly allotment farms and direct-to-consumer sales at farm stands, contributed to the mitigation of food security concerns in neighborhood communities. This means that urban agriculture could enhance the resilience of the urban food system at a time when the global food system has been disrupted due to a pandemic. This validates recent discussions about the potential of urban agriculture to facilitate food system resilience10. Furthermore, our findings imply that the types of urban agriculture employed matter in determining the degree of contribution to food system resilience.To summarize the overall results, urban agriculture in walkable neighborhoods bore fruit for health and food system resilience during the COVID-19 pandemic. However, different types of urban agriculture exhibited varying associations with health and resilience. Allotment farms were positively related to all of the following: subjective well-being, physical activity, and food security concerns, both during the state of emergency and in the future. Home gardens were positively related to subjective well-being, physical activity, and food security concerns only during the state of emergency. Farm stands were positively related to physical activity and food security concerns both during the state of emergency and in the future.These differences may be due to the characteristics of the respective spaces. It is suggested that this diversity of urban agriculture has led to different types of people benefiting from various kinds of urban agriculture. Allotment farms were found to be associated with high subjective well-being, physical activity, and food security, but they may not be feasible for those who do not have enough physical strength because users are responsible for cultivating their lots, which measure 10–30 square meters40. In contrast, home gardens can be created even by those who are not confident in their physical strength. In fact, our study showed that women and older people engaged in home gardening more than men and younger people. In addition, direct-to-consumer sales at farm stands are the easiest way to obtain local fresh foods for those who do not have the time and space for allotment farms and home gardens. The need for urban agriculture has been argued in many countries2,3. However, little attention has been paid to its scale, accessibility, and diversity. Our study suggests that it is worthwhile to create diverse food production spaces within walkable neighborhoods while considering the diversity of people who access these spaces.Compared to other urban greenery and food retailers, the benefits of urban agriculture on subjective well-being and food security could be greaterCompared to the use of other urban green spaces, including urban parks, our results indicated that self-cultivation at allotment farms and home gardens was more strongly associated with subjective well-being. Previous studies have offered limited perspectives on the differences among various types of urban green spaces33. Our study further suggests that urban parks, allotment farms, and home gardens are differently associated with human health. However, as the reason was not determined, further research is needed.Furthermore, compared to other food retailers, such as supermarkets, convenience stores, and co-op deliveries, allotment farms and farm stands were more strongly associated with less anxiety about fresh food availability in the future. The availability of local fresh foods within walkable neighborhoods might have mitigated food security concerns because residents could grow food by themselves or directly observe farmers’ production processes, which may have made the difference from purchasing at places where the food systems were not visible.Flexibility in work style might promote urban agriculture in walkable neighborhoodsThere was an association between work style—working from home—and access to local food. According to the Ministry of Health, Labor and Welfare (https://www.mhlw.go.jp/english), 52% of Tokyo office workers worked from home during the first emergency declaration. Long commute times and high train congestion rates have been a problem in Tokyo suburbs, but remote workers have gained more time at and around their homes by reducing their commute times, increasing their opportunities to access local food in their walkable neighborhoods. Those who worked from home sought outdoor activities for refreshment and exercise and used a variety of urban green spaces during the pandemic49. Allotment farms and home gardens might be used as such urban green spaces. This result is consistent with previous studies assessing the characteristics of Canadian gardeners during the COVID-19 pandemic28,30.Until now, urban planners and policymakers have rarely taken work style into account. However, the flexibility of work styles and work hours may bring new insights; for example, those who work from home may become important players in urban agriculture. It has been pointed out that cities have a large hidden potential for urban agriculture by cultivating underused lands50. Our study suggests that such underused lands could be converted into productive urban landscapes for remote workers to engage in farming or gardening in between jobs as a hobby or as a side business.Food equity might be improved by urban agriculture in walkable neighborhoodsLocal fresh food is generally considered more expensive than junk food in high-income countries, creating social issues of food inequity. Therefore, past discussions on urban agriculture and food security have focused primarily on low-income households in socioeconomically disadvantaged areas24,25,26.In contrast, our study covered people from all income groups and found no statistically significant relationship between access to local food and income. This finding might be due to two urban cultural backgrounds regarding local food in Tokyo, that is, accessibility and affordability. First, residential segregation by income levels is not noteworthy in Tokyo and people from various income brackets live mixed in the same neighborhoods51. Therefore, most urban residents living in the suburbs have geographically equitable opportunities to access local foods. Second, local foods sold at farm stands are affordable. Prices are almost the same or cheaper than buying food at food retailers. While prices increase because of middleman margins related to shipping in the wholesale market, such increases are unnecessary when selling directly to consumers at farm stands. In addition, the allotment farm lots are not expensive to rent, particularly those operated by local municipalities (Supplementary Note 1).These two backgrounds make local fresh food physically and economically accessible to consumers of all income levels, resulting in food equity. This is particularly important because the concept of food system resilience includes the equitability perspective27.The integration of urban agriculture into walkable neighborhoods is a fruitful wayWhile the current discussion on walkable neighborhoods does not emphasize urban agriculture, our evidence indicated its effectiveness. The concept of walkable neighborhoods (e.g., the 15-min city model) stresses the decarbonization benefit of limiting vehicle travel, as well as the health benefits of promoting walking and cycling13,14,15,16. In addition, our research indicated that urban agriculture in walkable neighborhoods benefited health and well-being by increasing recreational outdoor opportunities to neighborhood communities, including remote workers. It also contributed to food system resilience by providing local foods to all people, including low-income households, when the global food system was disrupted due to the pandemic. Furthermore, recent studies on urban agriculture reported the decarbonization benefit of reducing carbon footprints in food production and distribution7,8. Small-scale and community-based urban agriculture in walkable neighborhoods might especially bring this benefit because neighborhood communities travel to farms on foot or by bicycle, which means almost no emission by distribution. While urban green spaces have various health benefits32,33,34,35, urban agriculture also contributes to food system resilience as well as carbon emission reduction, which makes it unique.Urban agriculture was once considered a failure of urban planning in Japan because it symbolized uncontrolled sprawl. This is analogous to the Western view, as urban agriculture was once considered the ultimate oxymoron1. However, our empirical evidence suggests that the urban‒rural mixture at neighborhood scales is a reasonable urban form that contributes to the resilience of the urban food system and to the health and well-being of neighborhood communities. It is no longer a failure of urban planning but a legacy of urban sprawl in the current urban context.Our study showed that integrating urban agriculture into walkable neighborhoods is a fruitful way of creating healthier cities and developing more resilient urban food systems during times of uncertainty. In cities where there is no farmland in intraurban areas, it would be considered effective to utilize underused spaces such as vacant lots and rooftops as productive urban landscapes. In growing cities where urban areas are still expanding, it would be advantageous to conserve agricultural landscapes within their urban fabrics. Our study could provide referential insights and robust evidence for urban policy to integrate urban agriculture into walkable neighborhoods.This study has potential limitations, including the timing of the survey and the measurement method that was utilized. We conducted the survey between June 4 and 8, 2020, just after the end of the first declaration of a state of emergency by the Japanese government. During this period, the main cultivation activities were planting and growing, and the harvest was just beginning. This seasonal constraint may have influenced the results. Because the survey was conducted during the pandemic, we used subjective methods to measure health and well-being status. However, the results might be different using objective methods52, thus further research is necessary. In addition, a longitudinal study is needed to determine whether the trends observed in this study were specific to the emergency period or whether they will persist after the COVID-19 pandemic. More

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    Bagarius bagarius, and Eichhornia crassipes are suitable bioindicators of heavy metal pollution, toxicity, and risk assessment

    Analytical method validationThe results of the precision study with relative standard deviation (RSD), and accuracy are shown in Table 1. Through the precision study we found the value of RSD as less than 5%. Moreover, accuracy was done with percent recovery experiments. The results showed that the percentage recoveries for spiked samples were in the range of 95.7–103.7%.Table 1 Shows percent (%) recovery and relative standard deviation.Full size tablePhysicochemical properties and water quality indexThe investigations of the water quality properties of the Narora channel are shown in Table 2. The temperature, TDS, turbidity, and alkalinity were within the standards of the country18 and WHO19 (taken from UNEPGEMS). While pH and dissolved oxygen (D.O) were above the recommended standards indicating poor water quality. Moreover, the detected heavy metals were in the following order Ni  > Fe  > Cd  > Zn  > Cr  > Cu  > Mn. Among these heavy metals Mn, Cu, and Zn were within the recommended limits whereas Cr, Fe, Ni, and Cd were crossing the limits18 contributing to the poor quality. Furthermore, the WQI calculation will give more insights into the overall quality of water as it explains the combined effect of several physicochemical properties12. Its calculation is done simply by converting numerous variables of water quality into a single number12,20. In addition to this, WQI simplifies all the data and helps in clarifying water quality issues by combining the complex data and producing a score that shows the status of water quality2,12,21. The WQI classifies water quality status into five groups such as if WQI  Cu  > Zn  > Fe  > Zn  > Ni  > Cr from root to stalk; and Mn  > Cd  > Zn  > Cu  > Fe  > Ni  > Cr from stalk to leaves.Table 5 Heavy metal concentrations in Eichhornia crassipes (mg/kg.dw).Full size tableFigure 3MPI values in E. crassipes.Full size imageTable 6 Bioaccumulation factor (BAF), transfer factor (TF), and mobility factor (MF) in plant E. crassipes.Full size tableThese factors BAF, TF, and MF are utilized to monitor the level of anthropogenic pollution in plants and their surrounding medium2,15,32,34,35. BAF shows the concentrations of heavy metals bioaccumulated by plants from the water. If the BAF  > 1 it indicates hyperaccumulation36. So, in the present study, all the concerned heavy metals were hyperaccumulated in the plant. The TF elucidates the capability of the plant to translocate the accumulated metals to its other parts. The roots of E. crassipes showed the highest translocation capacity for Ni (1.57) as well as Zn (1.30) to other parts. If the value of TF exceeds 1, then it represents the high accumulation efficiency37,38, therefore, plants will be considered as the hyperaccumulators for the Ni and Zn. Although the Cd was the highest accumulated metal in the plant, it could have been because of its may be because of its low TF. Whereas, TF values lower than 1 for Cr, Mn, Fe, Cu, and Cd pointed out that this plant’s roots act as a non-hyperaccumulator for these heavy metals. Furthermore, the highest MF values were depicted for Mn in both cases which reflects that E. crassipes can suitably be used for phytoextraction of Mn as well as for Cd, Zn, Fe, Ni, and Cu. The BAF, TF, and MF of Cr are low in the present study, which implies that roots are limiting the Cr. Moreover, if the BAF ≤ 1.00 then it shows the capability of absorption only rather than accumulation36,37. In addition, if the values of BAF, TF, and MF exceed 1, plants can also work for phytoextraction. Furthermore, if the BAF  > 1 and TF  More