Philippa Kaur

Saponari, M. et al. Infectivity and transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. J. Econ. Entomol. 107, 1316–1319. https://doi.org/10.1603/EC14142 (2014).Article 

Google Scholar 
Cornara, D., Bosco, D. & Fereres, A. Philaenus spumarius: When an old acquaintance becomes a new threat to European agriculture. J. Pest Sci. 91, 957–972. https://doi.org/10.1007/s10340-018-0966-0 (2018).Article 

Google Scholar 
Weaver, C. R. & King, D. Meadow spittlebug, Philaenus leucophthalmus (L.). Ohio Agric. Exp. Stn. Res. Bull. 741, 258 (1954).
Google Scholar 
Halkka, A., Halkka, L., Halkka, O., Roukka, K. & Pokki, J. Lagged effects of North Atlantic Oscillation on spittlebug Philaenus spumarius (Homoptera) abundance and survival. Glob. Change Biol. 12, 2250–2262. https://doi.org/10.1111/j.1365-2486.2006.01266.x (2006).Article 

Google Scholar 
Cruaud, A. et al. Using insects to detect, monitor and predict the distribution of Xylella fastidiosa: A case study in Corsica. Sci. Rep. 8, 15628. https://doi.org/10.1038/s41598-018-33957-z (2018).Article 
CAS 

Google Scholar 
Godefroid, M. et al. Climate tolerances of Philaenus spumarius should be considered in risk assessment of disease outbreaks related to Xylella fastidiosa. J. Pest Sci. 2021, 1–14. https://doi.org/10.1007/s10340-021-01413-z (2021).Article 

Google Scholar 
Farigoule, P. et al. Vectors as sentinels: Rising temperatures increase the risk of Xylella fastidiosa outbreaks. Biology 11, 1299. https://doi.org/10.3390/biology11091299 (2022).Article 

Google Scholar 
Drosopoulos, S. & Asche, M. Biosystematic studies on the spittlebug genus Philaenus with the description of a new species. Zool. J. Linn. Soc. 101, 169–177. https://doi.org/10.1111/j.1096-3642.1991.tb00891.x (1991).Article 

Google Scholar 
Godefroid, M. & Durán, J. M. Composition of landscape impacts the distribution of the main vectors of Xylella fastidiosa in southern Spain. J. Appl. Entomol. 146, 666–675. https://doi.org/10.1111/jen.13003 (2022).Article 

Google Scholar 
Karban, R. & Strauss, S. Y. Physiological tolerance, climate change, and a northward range shift in the spittlebug, Philaenus spumarius. Ecol. Entomol. 29, 251–254. https://doi.org/10.1111/j.1365-2311.2004.00576.x (2004).Article 

Google Scholar 
Chmiel, S. M. & Wilson, M. C. Estimation of the lower and upper developmental threshold temperatures and duration of the nymphal stages of the meadow Spittlebug, Philaenus spumarius. Environ. Entomol. 8, 682–685. https://doi.org/10.1093/ee/8.4.682 (1979).Article 

Google Scholar 
Yurtsever, S. On the polymorphic meadow spittlebug, Philaenus spumarius (L.) (Homoptera: Cercopidae). Turk. J. Zool. 24, 447–460 (2000).
Google Scholar 
Ahmed, D. D. & Davidson, R. H. Life history of the meadow spittlebug in Ohio. J. Econ. Entomol. 43, 905–908. https://doi.org/10.1093/jee/43.6.905 (1950).Article 

Google Scholar 
Whittaker, J. B. Cercopid spittle as a microhabitat. Oikos 21, 59–64. https://doi.org/10.2307/3543839 (1970).Article 

Google Scholar 
Drosopoulos, S. New data on the nature and origin of colour polymorphism in the spittlebug genus Philaenus (Hemiptera: Aphorophoridae). Ann. Soc. Entomol. Fr. NS 39, 31–42. https://doi.org/10.1080/00379271.2003.10697360 (2003).Article 

Google Scholar 
Bodino, N. et al. Phenology, seasonal abundance, and host-plant association of spittlebugs (Hemiptera: Aphrophoridae) in vineyards of Northwestern Italy. Insects 12, 1012. https://doi.org/10.3390/insects12111012 (2021).Article 

Google Scholar 
Cornara, D. et al. Natural areas as reservoir of candidate vectors of Xylella fastidiosa. Bull. Insectol. 74, 173–180 (2021).
Google Scholar 
Gargani, E. et al. A five-year survey in Tuscany (Italy) and detection of Xylella fastidiosa subspecies multiplex in potential insect vectors, collected in Monte Argentario. Redia 104, 75–88. https://doi.org/10.19263/REDIA-104.21.09 (2021).Article 

Google Scholar 
Morente, M. et al. Distribution and relative abundance of insect vectors of Xylella fastidiosa in olive groves of the iberian peninsula. Insects 9, 175. https://doi.org/10.3390/insects9040175 (2018).Article 

Google Scholar 
Delong, D. et al. Spittle-insect vectors of Pierce’s disease virus. I. Characters, distribution, and food plants. Hilgardia 19, 339–356 (1950).Article 

Google Scholar 
Bodino, N. et al. Phenology, seasonal abundance and stage-structure of spittlebug (Hemiptera: Aphrophoridae) populations in olive groves in Italy. Sci. Rep. 9, 1–17. https://doi.org/10.1038/s41598-019-54279-8 (2019).Article 
CAS 

Google Scholar 
Wiegert, R. G. Population energetics of meadow spittlebugs (Philaenus spumarius L.) as affected by migration and habitat. Ecol. Monogr. 34, 217–241. https://doi.org/10.2307/1948501 (1964).Article 

Google Scholar 
Dongiovanni, C. et al. Plant selection and population trend of spittlebug immatures (Hemiptera: Aphrophoridae) in olive groves of the Apulia region of Italy. J. Econ. Entomol. 112, 67–74. https://doi.org/10.1093/jee/toy289 (2019).Article 

Google Scholar 
Bodino, N. et al. Spittlebugs of mediterranean olive groves: Host-plant exploitation throughout the year. Insects 11, 130. https://doi.org/10.3390/insects11020130 (2020).Article 

Google Scholar 
Villa, M., Rodrigues, I., Baptista, P., Fereres, A. & Pereira, J. A. Populations and host/non-host plants of spittlebugs nymphs in olive orchards from northeastern Portugal. Insects 11, 720. https://doi.org/10.3390/insects11100720 (2020).Article 

Google Scholar 
Antonatos, S. et al. Seasonal appearance, abundance, and host preference of Philaenus spumarius and Neophilaenus campestris (Hemiptera: Aphrophoridae) in olive groves in Greece. Environ. Entomol. 50, 1474–1482. https://doi.org/10.1093/ee/nvab093 (2021).Article 

Google Scholar 
Hasbroucq, S., Casarin, N., Ewelina, C., Bragard, C. & Grégoire, J.-C. Distribution, adult phenology and life history traits of potential insect vectors of Xylella fastidiosa in Belgium. Belg. J. Entomol. 92, 2569 (2020).
Google Scholar 
Mesmin, X. et al. Interaction networks between spittlebugs and vegetation types in and around olive and clementine groves of Corsica; implications for the spread of Xylella fastidiosa. Agric. Ecosyst. Environ. 334, 107979. https://doi.org/10.1016/j.agee.2022.107979 (2022).Article 

Google Scholar 
Albre, J., García-Carrasco, J. M. & Gibernau, M. Ecology of the meadow spittlebug Philaenus spumarius in the Ajaccio region (Corsica)—I: Spring. Bull. Entomol. Res. 111, 246–256. https://doi.org/10.1017/S0007485320000711 (2021).Article 

Google Scholar 
Andersson, P., Löfstedt, C. & Hambäck, P. A. Insect density–plant density relationships: A modified view of insect responses to resource concentrations. Oecologia 173, 1333–1344. https://doi.org/10.1007/s00442-013-2737-1 (2013).Article 

Google Scholar 
Hambäck, P. A., Inouye, B. D., Andersson, P. & Underwood, N. Effects of plant neighborhoods on plant–herbivore interactions: Resource dilution and associational effects. Ecology 95, 1370–1383. https://doi.org/10.1890/13-0793.1 (2014).Article 

Google Scholar 
Otway, S. J., Hector, A. & Lawton, J. H. Resource dilution effects on specialist insect herbivores in a grassland biodiversity experiment. J. Anim. Ecol. 74, 234–240 (2005).Article 

Google Scholar 
Lago, C. et al. Flight performance and the factors affecting the flight behaviour of Philaenus spumarius the main vector of Xylella fastidiosa in Europe. Sci. Rep. 11, 17608. https://doi.org/10.1038/s41598-021-96904-5 (2021).Article 
CAS 

Google Scholar 
Casarin, N. et al. Investigating dispersal abilities of Aphrophoridae in European temperate regions to assess the threat of potential Xylella fastidiosa-based pathosystems. J. Pest Sci. https://doi.org/10.1007/s10340-022-01562-9 (2022).Article 

Google Scholar 
Bodino, N. et al. Dispersal of Philaenus spumarius (Hemiptera: Aphrophoridae), a vector of Xylella fastidiosa, in olive grove and meadow agroecosystems. Environ. Entomol. 50, 267–279. https://doi.org/10.1093/ee/nvaa140 (2020).Article 
CAS 

Google Scholar 
Santoiemma, G., Tamburini, G., Sanna, F., Mori, N. & Marini, L. Landscape composition predicts the distribution of Philaenus spumarius, vector of Xylella fastidiosa, in olive groves. J. Pest. Sci. 92, 1101–1109. https://doi.org/10.1007/s10340-019-01095-8 (2019).Article 

Google Scholar 
Cappellari, A. et al. Spatio-temporal dynamics of vectors of Xylella fastidiosa subsp. pauca across heterogeneous landscapes. Entomol. Gen. 42, 515–521. https://doi.org/10.1127/entomologia/2022/1427 (2022).Article 

Google Scholar 
Avosani, S., Tattoni, C., Mazzoni, V. & Ciolli, M. Occupancy and detection of agricultural threats: The case of Philaenus spumarius, European vector of Xylella fastidiosa. Agric. Ecosyst. Environ. 324, 107707. https://doi.org/10.1016/j.agee.2021.107707 (2022).Article 

Google Scholar 
Allier, C. & Lacoste, A. Processus dynamiques de reconstitution dans la série du Quercus ilex en Corse. In Vegetation Dynamics in Grasslans, Healthlands and Mediterranean Ligneous Formations 83–91 (Springer, 1981).Delbosc, P., Bioret, F. & Panaïotis, C. Plant landscape of Corsica: Typology and mapping plant landscape of Cap Corse region and Biguglia Pond (Springer Nature, 2020).Book 

Google Scholar 
Chessel, D., Dufour, A.-B. & Thioulouse, J. The ade4 package—I: One-table methods. R. News 4, 5–10 (2004).
Google Scholar 
Biedermann, R. & Niedringhaus, R. The Plant-and Leafhoppers of Germany: Identification Key to All Species (Wabv Fründ, 2009).
Google Scholar 
Stöckmann, M., Biedermann, R., Nickel, H. & Niedringhaus, R. The Nymphs of the Planthoppers and Leafhoppers of Germany (WABV, 2013).
Google Scholar 
INRAE-CBGP. Arthemis DB@se – ARTHropod Ecology, Molecular Identification and Systematics. https://arthemisdb.supagro.inrae.frhttps://doi.org/10.15454/TBGRIB. Accessed 2021.Xu, T. & Hutchinson, M. ANUCLIM version 6.1 user guide. Aust. Natl. Univ. Fenner Sch. Environ. Soc. Canberra 2011, 256 (2011).
Google Scholar 
Quintana-Seguí, P. et al. Analysis of near-surface atmospheric variables: Validation of the SAFRAN analysis over France. J. Appl. Meteorol. Climatol. 47, 92–107. https://doi.org/10.1175/2007JAMC1636.1 (2008).Article 

Google Scholar 
Hijmans, R. J., Phillips, S., Leathwick, J. & Elith, J. Dismo: Species Distribution Modeling https://CRAN.R-project.org/package=dismo (2017).Faraway, J. J. Extending the Linear Model with R: Generalized Linear, Mixed Effects and Nonparametric Regression Models (Chapman and Hall/CRC, 2006).MATH 

Google Scholar 
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9, 378–400. https://doi.org/10.3929/ethz-b-000240890 (2017).Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing https://www.R-project.org/ (2019).Hardin, J. W. & Hilbe, J. M. Generalized Linear Models and Extensions 4th edn. (Stata Press, 2018).MATH 

Google Scholar 
Harrison, X. A. Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2, e616. https://doi.org/10.7717/peerj.616 (2014).Article 

Google Scholar 
Bolker, B. M. et al. Generalized linear mixed models: A practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135. https://doi.org/10.1016/j.tree.2008.10.008 (2009).Article 

Google Scholar 
Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models https://CRAN.R-project.org/package=DHARMa (2020).Lüdecke, D., Ben-Shachar, M. S., Patil, I., Waggoner, P. & Makowski, D. performance: An R package for assessment, comparison and testing of statistical models. J. Open Sourc. Softw. 6, 3139. https://doi.org/10.21105/joss.03139 (2021).Article 

Google Scholar 
Fox, J. & Weisberg, S. An {R} Companion to Applied Regression Third edn, https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (Sage, Thousand Oaks CA, 2019).Lenth, R. V. Emmeans: Estimated Marginal Means, Aka Least-Squares Means https://CRAN.R-project.org/package=emmeans (2021).Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363. https://doi.org/10.1002/bimj.200810425 (2008).Article 
MATH 

Google Scholar 
Fernández-Mazuecos, M. & Vargas, P. Ecological rather than geographical isolation dominates Quaternary formation of Mediterranean Cistus species. Mol. Ecol. 19, 1381–1395. https://doi.org/10.1111/j.1365-294X.2010.04549.x (2010).Article 
CAS 

Google Scholar 
Berenbaum, M. R. & Feeny, P. P. 1. Chemical mediation of host-plant specialization: The papilionid paradigm. In Specialization, Speciation, and Radiation (ed. Tilmon, K.) 3–19 (University of California Press, 2008). https://doi.org/10.1525/california/9780520251328.003.0001.Kapantaidaki, D. E., Antonatos, S., Evangelou, V., Papachristos, D. P. & Milonas, P. Genetic and endosymbiotic diversity of Greek populations of Philaenus spumarius, Philaenus signatus and Neophilaenus campestris, vectors of Xylella fastidiosa. Sci. Rep. 11, 3752. https://doi.org/10.1038/s41598-021-83109-z (2021).Article 
CAS 

Google Scholar 
Mesmin, X. et al. Ooctonus vulgatus (Hymenoptera, Mymaridae), a potential biocontrol agent to reduce populations of Philaenus spumarius (Hemiptera, Aphrophoridae) the main vector of Xylella fastidiosa in Europe. PeerJ 8, e8591. https://doi.org/10.7717/peerj.8591 (2020).Article 

Google Scholar 
Denancé, N. et al. Several subspecies and sequence types are associated with the emergence of Xylella fastidiosa in natural settings in France. Plant Pathol. 66, 1054–1064. https://doi.org/10.1111/ppa.12695 (2017).Article 
CAS 

Google Scholar 
EFSA, Delbianco, A., Gibin, D., Pasinato, L. & Morelli, M. Update of the Xylella spp host plant database—systematic literature search up to 31 December 2020. EFSA J. 19, 6. https://doi.org/10.2903/j.efsa.2021.6674 (2021).Article 

Google Scholar 
Soubeyrand, S. et al. Inferring pathogen dynamics from temporal count data: The emergence of Xylella fastidiosa in France is probably not recent. New Phytol. 219, 824–836. https://doi.org/10.1111/nph.15177 (2018).Article 

Google Scholar 
Roy, J. & Sonié, L. Germination and population dynamics of Cistus species in relation to fire. J. Appl. Ecol. 29, 647–655. https://doi.org/10.2307/2404472 (1992).Article 

Google Scholar 
Whittaker, J. B. Density regulation in a population of Philaenus spumarius (L.) (Homoptera: Cercopidae). J. Anim. Ecol. 42, 163–172. https://doi.org/10.2307/3410 (1973).Article 

Google Scholar 
Chapman, D. et al. Improving knowledge of Xylella fastidiosa vector ecology: modelling vector occurrence and abundance in the wider landscape in Scotland. Project Final Report. PHC2020/04, Scotland’s Centre of Expertise for Plant Health (PHC) https://doi.org/10.5281/zenodo.6523478 (2022).Saponari, M., Giampetruzzi, A., Loconsole, G., Boscia, D. & Saldarelli, P. Xylella fastidiosa in olive in Apulia: Where we stand. Phytopathology 109, 175–186. https://doi.org/10.1094/PHYTO-08-18-0319-FI (2019).Article 
CAS 

Google Scholar 
López-Mercadal, J. et al. Collection of data and information in Balearic Islands on biology of vectors and potential vectors of Xylella fastidiosa (GP/EFSA/ALPHA/017/01). EFSA Supp. Publ. 18, 10. https://doi.org/10.2903/sp.efsa.2021.EN-6925 (2021).Article 

Google Scholar  More

Now consider a generalized model in which the species interactions are heterogeneous. A natural way of introducing heterogeneity in the system is by having a species diversify into subpopulations with different interaction strengths12,13,14,15. This way of modeling heterogeneity is useful as it can describe different kinds of heterogeneity. For example, the subpopulations could represent polymorphic traits that are genetically determined or result from plastic response to heterogeneous environments. A population could also be divided into local subpopulations in different spatial patches, which can migrate between patches and may face different local predators. We can also model different behavioral modes as subpopulations that, for instance, spend more time foraging for food or hiding from predators. We study several kinds of heterogeneity after we introduce a common mathematical framework. By studying these different scenarios using variants of the model, we show that our main results are not sensitive to the details of the model.We focus on the simple case where only the prey species splits into two types, (C_1) and (C_2), as illustrated in Fig. 1b. The situation is interesting when predator A consumes (C_1) more readily than predator B and B consumes (C_2) more readily than A (i.e., (a_1 / a_0 > b_1 / b_0) and (b_2 / b_0 > a_2 / a_0), which is equivalent to the condition that the nullclines of A and B cross, see section “Resources competition and nullcline analysis”). The arrows between (C_1) and (C_2) in Fig. 1b represent the exchange of individuals between the two subpopulations, which can happen by various mechanisms considered below. Such exchange as well as intraspecific competition between (C_1) and (C_2) result from the fact that the two prey types remain a single species.The system is now described by an enlarged Lotka-Volterra system with four variables, A, B, (C_1), and (C_2): $$begin{aligned} dot{A}&= varepsilon _A ,alpha _{A1} , A , C_1 + alpha _{A2} , A , C_2 – beta _A , A end{aligned}$$
(3a)
$$begin{aligned} dot{B}&= varepsilon _B , alpha _{B1} , B , C_1 + alpha _{B2} , B , C_2 – beta _B , B end{aligned}$$
(3b)
$$begin{aligned} dot{C_1}&= C_1 , (beta _C – alpha _{CC} , C)-alpha _{A1} , C_1 A-alpha _{B1} , C_1 B – sigma _1 , C_1 + sigma _2 , C_2 end{aligned}$$
(3c)
$$begin{aligned} dot{C_2}&= C_2 , (beta _C – alpha _{CC} , C) -alpha _{A2} , C_2 A -alpha _{B2} , C_2 B + sigma _1 , C_1 – sigma _2 , C_2 end{aligned}$$
(3d)
The parameters in these equations and their meanings are listed in Table 1. Here we assume that the prey types (C_1) and (C_2) have the same birth rate and intraspecific competition strength, but different interaction strengths with A and B. Note that (C_1) and (C_2) are connected by the (sigma _i) terms, which represent the exchange of individuals between these subpopulations through mechanisms studied below; these terms indicate a major difference between our model of a prey with intraspecific heterogeneity and other models of two prey species. For the convenience of analysis, we transform the variables (C_1) and (C_2) to another pair of variables C and (lambda), where (C equiv C_1 + C_2) is the total population of C as before, and (lambda equiv C_2 / (C_1 + C_2)) represents the composition of the population (Fig. 1c). After this transformation and rescaling of variables (described in “Methods”), the new dynamical system can be written as: $$begin{aligned} dot{A}&= A , big ( C , (a_1 (1-lambda ) + a_2 lambda ) – a_0 big ) end{aligned}$$
(4a)
$$begin{aligned} dot{B}&= B , big ( C , (b_1 (1-lambda ) + b_2 lambda ) – b_0 big ) end{aligned}$$
(4b)
$$begin{aligned} dot{C}&= C , big ( 1 – C – A (a_1 (1-lambda ) + a_2 lambda ) – B (b_1 (1-lambda ) + b_2 lambda ) big ) end{aligned}$$
(4c)
$$begin{aligned} dot{lambda }&= lambda (1-lambda ) , big ( A (a_1 – a_2) + B (b_1 – b_2) big ) + eta _1 (1-lambda ) – eta _2 lambda end{aligned}$$
(4d)
Here, (a_i) and (b_i) are the (rescaled) feeding rates of the predators on the prey type (C_i); (a_0) and (b_0) are the death rates of the predators as before; (eta _1) and (eta _2) are the exchange rates of the prey types (Table 1). The latter can be functions of other variables, representing different kinds of heterogeneous interactions that we study below. Notice that Eqs. (4a–4c) are equivalent to the homogeneous Eqs. (2a–2c) but with effective interaction strengths (a_text {eff} = (1-lambda ) , a_1 + lambda , a_2) and (b_text {eff} = (1-lambda ) , b_1 + lambda , b_2) that both depend on the prey composition (lambda) (Fig. 1c).Table 1 Model parameters (before/after rescaling) and their meanings.Full size tableThe variable (lambda) can be considered an internal degree of freedom within the C population. In all of the models we study below, (lambda) dynamically stabilizes to a special value (lambda ^*) (a bifurcation point), as shown in Fig. 3a. Accordingly, a new equilibrium point (P_N) appears (on the line (mathscr {L}) in Fig. 2), at which all three species coexist. For comparison, Fig. 3b shows the equilibrium points if (lambda) is held fixed at any other values, which all result in the exclusion of one of the predators. Thus, heterogeneous interactions give rise to a new coexistence phase (see Fig. 4 below) by bringing the prey composition (lambda) to the value (lambda ^*), instead of having to fine-tune the interaction strengths. The exact conditions for this new equilibrium to be stable are detailed in “Methods”.Figure 3(a) Time series of (lambda) for systems with each kind of heterogeneity. All three systems stabilize at the same (lambda ^*) value, which is the bifurcation point in panel (b). (b) Equilibrium population of each species (X = A), B, or C, with (lambda) held fixed at different values. Solid curves represent stable equilibria and dashed curves represent unstable equilibria (see Eq. (9) in “Methods”). The vertical dashed line is where (lambda = lambda ^*), which is also the bifurcation point. Notice that the equilibrium population of C is maximized at this point (for (a_1 > a_2) and (b_2 > b_1)). Parameters used here are ((a_0, a_1, a_2, b_0, b_1, b_2, rho , eta _1, eta _2, kappa ) = (0.25, 0.5, 0.2, 0.4, 0.2, 0.6, 0.5, 0.05, 0.05, 50)).Full size imageInherent heterogeneityWe first consider a scenario where individuals of the prey species are born as one of two types with a fixed ratio, such that a fraction (rho) of the newborns are (C_2) and ((1-rho )) are (C_1). This could describe dimorphic traits, such as the winged and wingless morphs in aphids12 or the horned and hornless morphs in beetles13. We call this “inherent” heterogeneity, because individuals are born with a certain type and cannot change in later stages of life. The prey type given at birth determines the individual’s interaction strength with the predators. This kind of heterogeneity can be described by Eq. (4d) with (eta _1 = rho (1-C)) and (eta _2 = (1-rho ) (1-C)) (see “Methods”).Figure 4Phase diagrams showing regions of parameter space identified by the stable equilibrium points. Yellow region represents (P_C) (predators A, B both extinct), red represents (P_A) (A excludes B), blue represents (P_B) (B excludes A), and green represents (P_N) (A, B coexist). The middle point (black dot) is where the preferences of the two predators are identical, (a_2/a_0=b_2/b_0) and (b_1/b_0=a_1/a_0). The coexistence phase appears in all three kinds of heterogeneity modeled here. (a–d) Inherent heterogeneity: Individuals of the prey population are born in two types with a fixed composition (rho). In the extreme cases of (rho = 0) and 1, the prey is homogeneous and there is no coexistence of the predators. (e–h) Reversible heterogeneity: Individual prey can switch types with fixed switching rates (eta _1) and (eta _2). As the switching rates increase, the coexistence region shrinks because the prey population becomes effectively homogeneous (the occasional green spots are numerical artifacts because the time to reach the equilibrium becomes long in this limit). (i–l) Adaptive heterogeneity: The switching rates (eta _i) dynamically adapt to the predator densities, so as to maximize the growth rate of the prey. As the sharpness (kappa) of the sigmoidal decision function is increased, the prey adapts more optimally and the region of coexistence expands. Parameters used here are ((a_0, a_1, b_0, b_2) = (0.3, 0.5, 0.4, 0.6)).Full size imageThe stable equilibrium of the system can be represented by phase diagrams that show the identities of the species at equilibrium. We plot these phase diagrams by varying the parameters (a_2) and (b_1) while keeping (a_1) and (b_2) constant. As shown in Fig. 4a–d, the equilibrium state depends on the parameter (rho). In the limit (rho = 0) or 1, we recover the homogeneous case because only one type of C is produced. The corresponding phase diagrams (Fig. 4a, d) contain only two phases where either of the predators is excluded, illustrating the competitive exclusion principle. For intermediate values of (rho), however, there is a new phase of coexistence that separates the two exclusion phases (Fig. 4b, c). There are two such regions of coexistence, which touch at a middle point and open toward the bottom left and upper right, respectively. The middle point is at ((a_2/a_0 = b_2/b_0, b_1/b_0 = a_1/a_0)), where the feeding preferences of the two predators are identical (hence their niches fully overlap). Towards the origin and the far upper right, the predators consume one type of C each (hence their niches separate). The coexistence region in the bottom left is where the feeding rates of the predators are the lowest overall. There can be a region (yellow) where both predators go extinct, if their primary prey type alone is not enough to sustain each predator. Increasing the productivity of the system by increasing the birth rate ((beta _C)) of the prey eliminates this extinction region, whereas lowering productivity causes the extinction region to take over the lower coexistence region. Because the existence and identity of the phases is determined by the configuration of the equilibrium points (Fig. 2, see also section “Mathematical methods”), the qualitative shape of the phase diagram is not sensitive to changes of parameter values.The new equilibrium is not only where the predators A and B can coexist, but also where the prey species C grows to a larger density than what is possible for a homogeneous population. This is illustrated in Fig. 3b, which shows the equilibrium population of C if we hold (lambda) fixed at different values. The point (lambda = lambda ^*) is where the system with a dynamic (lambda) is stable, and also where the population of C is maximized (when A and B prefer different prey types). That means the population automatically stabilizes at the optimal composition of prey types. Moreover, the value of (C^*) at this coexistence point can even be larger than the equilibrium population of C when there is only one predator A or B. This is discussed further in section “Multiple-predator effects and emergent promotion of prey”. These results suggest that heterogeneity in interaction strengths can potentially be a strategy for the prey population to leverage the effects of multiple predators against each other to improve survival.Reversible heterogeneityWe next consider a scenario where individual prey can switch their types. This kind of heterogeneity can model reversible changes of phenotypes, i.e., trait changes that affect the prey’s interaction with predators but are not permanent. For example, changes in coat color or camouflage14,16,17, physiological changes such as defense15, and biomass allocation among tissues18,19. One could also think of the prey types as subpopulations within different spatial patches, if each predator hunts at a preferred patch and the prey migrate between the patches20,21. With some generalization, one could even consider heterogeneity in resources, such as nutrients located in different places, that can be reached by primary consumers, such as swimming phytoplankton22. We can model this “reversible” kind of heterogeneity by introducing switching rates from one prey type to the other. In Eq. (4d), (eta _1) and (eta _2) now represent the switching rates per capita from (C_1) to (C_2) and from (C_2) to (C_1), respectively. Here we study the simplest case where both rates are fixed.In the absence of the predators, the natural composition of the prey species given by the switching rates would be (rho equiv eta _1 / (eta _1 + eta _2)), and the rate at which (lambda) relaxes to this natural composition is (gamma equiv eta _1 + eta _2). Compared to the previous scenario where we had only one parameter (rho), here we have an additional parameter (gamma) that modifies the behavior of the system. Fig. 4e–h shows phase diagrams for the system as (rho) is fixed and (gamma) varies. We again find the new equilibrium (P_N) where all three species coexist. When (gamma) is small, the system has a large region of coexistence. As (gamma) is increased, this region is squeezed into a border between the two regions of exclusion, where the slope of the border is given by (eta _1/eta _2) as determined by the parameter (rho). However, this is different from the exclusion we see in the case of inherent heterogeneity, which happens only for (rho rightarrow 0) or 1, where the borders are horizontal or vertical (Fig. 4a,d). Here the predators exclude each other despite having a mixture of prey types in the population.This special limit can be understood as follows. For a large (gamma), (lambda) is effectively set to a constant value equal to (rho), because it has a very fast relaxation rate. In other words, the prey types exchange so often that the population always maintains a constant composition. In this limit, the system behaves as if it were a homogeneous system with effective interaction strengths (a_text {eff} = (1-rho ) , a_1 + rho , a_2) and (b_text {eff} = (1-rho ) , b_1 + rho , b_2). As in a homogeneous system, there is competitive exclusion between the predators instead of coexistence. This demonstrates that having a constant level of heterogeneity is not sufficient to cause coexistence. The overall composition of the population must be able to change dynamically as a result of population growth and consumption by predators.An interesting behavior is seen when we examine a point inside the shrinking coexistence region as (gamma) is increased. Typical trajectories of the system for such parameter values are shown in Fig. 5. As (gamma) increases, the system relaxes to the line (mathscr {L}) quickly, then slowly crawls along it towards the final equilibrium point (P_N). This is because increasing (gamma) increases the speed that (lambda) relaxes to (lambda ^*), and when (lambda rightarrow lambda ^*), (mathscr {L}) becomes marginally stable. Therefore, the attraction to (mathscr {L}) in the perpendicular direction is strong, but the attraction towards the equilibrium point along (mathscr {L}) is weak. This leads to a long transient behavior that makes the system appear to reach no equilibrium in a limited time23,24. It is especially true when there is noise in the dynamics, which causes the system to diffuse along (mathscr {L}) with only a weak drift towards the final equilibrium (Fig. 5). Thus, the introduction of a fast timescale (quick relaxation of (lambda) due to a large (gamma)) actually results in a long transient.Figure 5Trajectories of the system projected in the A-B plane, with parameters inside the coexistence region (by holding the position of (P_N) fixed). As (gamma) increases, the system tends to approach the line (mathscr {L}) quickly and then crawl along it. The grey trajectory is with independent Gaussian white noise ((sim mathscr {N}(0,0.5))) added to each variable’s dynamics. Noise causes the system to diffuse along (mathscr {L}) for a long transient period before coming to the equilibrium point (P_N). Parameters used here are ((a_0, a_1, a_2, b_0, b_1, b_2) = (0.2, 0.8, 0.5, 0.2, 0.6, 0.9)), chosen to place (P_N) away from the middle of (mathscr {L}) to show the trajectory drifting toward the equilibrium.Full size imageAdaptive heterogeneityA third kind of heterogeneity we consider is the change of interactions in time. By this we mean an individual can actively change its interaction strength with others in response to certain conditions. This kind of response is often invoked in models of adaptive foraging behavior, where individuals choose appropriate actions to maximize some form of fitness25,26. For example, we may consider two behaviors, resting and foraging, as our prey types. Different predators may prefer to strike when the prey is doing different things. In response, the prey may choose to do one thing or the other depending on the current abundances of different predators. Such behavioral modulation is seen, for example, in systems of predatory spiders and grasshoppers27. Phenotypic plasticity is also seen in plant tissues in response to consumers28,29,30.This kind of “adaptive” heterogeneity can be modeled by having switching rates (eta _1) and (eta _2) that are time-dependent. Let us assume that the prey species tries to maximize its population growth rate by switching to the more favorable type. From Eq. (4c), we see that the growth rate of C depends linearly on the composition (lambda) with a coefficient (u(A,B) equiv (a_1 – a_2) A + (b_1 – b_2) B). Therefore, when this coefficient is positive, it is favorable for C to increase (lambda) by switching to type (C_2). This can be achieved by having a positive switching rate (eta _2) whenever (u(A,B) > 0). Similarly, whenever (u(A,B) < 0), it is favorable for C to switch to type (C_1) by having a positive (eta _1). In this way, the heterogeneity of the prey population constantly adapts to the predator densities. We model such adaptive switching by making (eta _1) and (eta _2) functions of the coefficient u(A, B), e.g., (eta _1(u) = 1/(1+mathrm {e}^{kappa u})) and (eta _2(u) = 1/(1+mathrm {e}^{-kappa u})). The sigmoidal form of the functions means that the switching rate in the favorable direction for C is turned on quickly, while the other direction is turned off. The parameter (kappa) controls the sharpness of this transition.Phase diagrams for the system with different values of (kappa) are shown in Fig. 4i–l. A larger (kappa) means the prey adapts its composition faster and more optimally, which causes the coexistence region to expand. In the extreme limit, the system changes its dynamics instantaneously whenever it crosses the boundary where (u(A,B) = 0), like in a hybrid system31. Such a system can still reach a stable equilibrium that lies on the boundary, if the flow on each side of the boundary points towards the other side32. This is what happens in our system and, interestingly, the equilibrium is the same three-species coexistence point (P_N) as in the previous scenarios. The region of coexistence turns out to be largest in this limit (Fig. 4l).Our results suggest that the coexistence of the predators can be viewed as a by-product of the prey’s strategy to maximize its own benefit. The time-dependent case studied here represents a strategy that involves the prey evaluating the risk posed by different predators. This is in contrast to the scenarios studied above, where the prey population passively creates phenotypic heterogeneity regardless of the presence of the predators. These two types of behavior are analogous to the two strategies studied for adaptation in varying environments, i.e., sensing and bet-hedging33,34. The former requires accessing information about the current environment to make optimal decisions, whereas the latter relies on maintaining a diverse population to reduce detrimental effects caused by environmental changes. Here the varying abundances of the predators play a similar role as the varying environment. From this point of view, the heterogeneous interactions studied here can be a strategy of the prey species that is evolutionarily favorable. More

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

Himalayan marmot habitat analysisThe environmental factors including temperature, vegetation and elevation are the key drivers for the wildlife in alpine ecosystems32. Specific landform attributes such as slope and elevation and vegetation cover affect the population and burrowing of rodents33. For example, rodent burrows in the Western Usambara Mountains in Tanzania were only found at an elevation of above 1600 m33. However, the Himalayan marmot seems to prefer to inhabit areas with low elevation and high land surface temperature34. In this study, the data showed that 76.25% of the Himalayan marmots were found in areas with elevation values of 3400–4600 m. The majority of marmots were found in areas with slopes of 5–20° and vegetation cover higher than 60%. Most marmots were found in alpine meadows, a few were found in temperate grasslands and alpine grasslands, and none were found in other grassland types.Preliminary statistical analysis of vegetation cover, grass type, vegetation type, and Himalayan marmot distribution sample sites obtained using spatial geographic information technology revealed that the meadow grassland areas with lush grass growth, more dominant plants, and abundant food had more marmots. When the vegetation cover reached 0.60–1.00, the number of marmot distribution sample sites was the highest. Dense grass is an ideal habitat and provides concealment for Himalayan marmots, and the abundant plant types provide sufficient food for marmots. In contrast, no marmots were distributed in the alpine scrub, coniferous forest, and alpine snow/ice covered areas where vegetation growth was poor, vegetation cover was low, and food was relatively scarce. Moreover, 70.24% of Himalayan marmots were found in alpine meadows with a wide variety of plant species, including Poaceae, Cyperaceae, and grasses. This finding indicated that alpine meadows are more suitable for Himalayan marmots and have more advantageous habitat conditions compared with other grassland types. The elevation of alpine meadows is 3236–5126 m, and the vegetation is mainly meadows with simple vegetation structure, substantial vegetation cover and dense vegetation growth, and a wide variety of plants, rich food, soft grass, and good palatability. Therefore, alpine meadows provide good natural habitats and foraging sites for marmots.Habitat selection of large rodents is influenced by a combination of vegetation cover availability, food availability, and population density35. Vegetation cover is an important parameter that describes vegetation communities and ecosystems and is closely related to vegetation quantity and productivity. The quality of habitat vegetation is an important factor that affects the spatial distribution of plateau rodents. Both feeding and concealment depend on vegetation, and the height and cover of edible plants and vegetation suitable for concealment determine the choice of vegetation type by marmots. Thus, vegetation cover becomes an important factor for habitat selection by marmots. Different grassland types determine different plant conditions, and selection of different vegetation conditions can increase the chances of survival and improve the reproductive success of marmots; therefore, grassland type is an important ecological factor in habitat selection by marmots. A study showed that the ecological factors affecting habitat selection of Himalayan marmots are mainly topography, anthropogenic disturbance, and vegetation8. Another study concluded that habitat selection by Himalayan marmots is closely related to elements such as topography, landform, temperature, precipitation, and vegetation24.The functions of burrows’ physical parameters is to protect the Himalayan marmots from natural enemies and bad weather36. There is clearly influence of slope on habitat selection by marmots. When the slope is large, wind is strong, and burrows are not well hidden; this makes them difficult to defend against enemies, unsafe for survival, and not conducive to hibernation during winter. In addition, Himalayan marmots prefer to burrow on sunny aspect, because the temperature is suitable and the vegetation is lush, which is suitable for marmots to breed. Therefore, the number of marmot burrows gradually decreases with increasing slope and ubac. Although flat and low-lying areas with small slopes are good for marmots to create dens, rainwater will easily flow into the dens during summer rainfall, which will kill marmots. Therefore, a suitable slope and sunny aspect are also very important for habitat selection by marmots.Application of the predictive spatial distribution map of Himalayan marmots in Qinghai provincePlague surveillance is the main measure used for plague prevention and control in China. Although we have made many improvements in plague surveillance, the traditional method of dragnet surveillance still consumes a lot of human and material resources, is inefficient. The pasture area of Qinghai province is approximately 380,000 km2, and the identified natural plague focus is approximately 180,000 km2; therefore, there is still 200,000 km2 of pasture where the distribution of Himalayan marmots and plague have not been identified. Currently, RS technology is widely used in the fields of mapping and ecological surveillance18,19,21,22,37.Applications of RS technology in areas such as malaria, dengue, schistosomiasis and plague have been previously reported27,37. Using GIS combined with remotely sensed data, Proches Hieronimo et al. found that the presence of small mammals was positively influenced by elevation, whereas the presence of fleas was clearly influenced by land management features, and thus these observations have positive implications for plague surveillance27. In this study, RS technology combined with field validations were used to determine the distribution and areas of different types of grasslands in Qinghai province, and the average density of Himalayan marmot distribution in different types of grasslands. The high-, low-, and very low-density areas of Himalayan marmot distribution were identified. The soil map, vegetation map, administrative map, and marmot density statistics were merged to form the spatial data and attribute data basis for the information system to map the distribution of Himalayan marmot and determine the area of Himalayan marmot distribution. Generally speaking, the occurrence of human plague epidemic is closely related to the local animal plague epidemic2. However, a large part of the high-density distribution of Himalayan marmots is located in uninhabited areas and the areas are generally sparsely populated, which also indicates that we should reasonably allocate plague prevention and control resources to areas where human plague is most likely to occur to prevent the occurrence of human plague epidemics.Field validation for verificationThrough field validation and information from local farmers and herdsmen, we confirmed that Himalayan marmots inhabited 68 sample sites in Tongde, Zeku, Guinan, Xunhua, Haiyan, Ulan, Qilian, Hualong, and Huzhu counties. Among them, Tongde, Zeku, Guinan, Xunhua, Haiyan, Ulan, and Qilian counties have all historically experienced marmot plague outbreaks and can be considered as reliable natural plague foci38. The data from this field validation are consistent with the previous survey data and the epidemic history of the counties in Qinghai province39.MAE can better reflect the actual number of errors in prediction values; the smaller the MAE value, the higher the prediction accuracy. The MAE derived from the field validation data was 0.1331 and the prediction accuracy was 0.8669. The accuracy of the predicted Himalayan marmot spatial distribution reached 87%, which indicated that the predicted probability map of the Himalayan marmot spatial distribution can better predict the potential marmot distribution.The predicted spatial distribution map of Himalayan marmot in Qinghai province was then compared with environmental information such as elevation, vegetation, grass type, slope, and aspect of 352 field survey sites. The obtained RS data showed that the prediction results were excellent, and the predicted spatial distribution map of Himalayan marmot in Qinghai province was drawn with high accuracy. The prediction map visually reflects the different density distribution of Himalayan marmots; this allows us to optimize the settings and reasonable spatial layout of animal plague surveillance sites and improve surveillance efficiency.Application of marmot information collection system V3.0Marmot information collection system V3.0 was developed based on the “3S” technology standardizing the collection of surveillance data, and makes the management and analysis of information more convenient and faster. This study revolutionized the traditional method of considering plague-stricken counties as the plague foci, and effectively reduces the work intensity of operators and improves the data collection efficiency. In 2016 and 2017, we applied this system to the animal plague surveillance tasks in the plague-stricken counties of Haidong, Hainan, and Haibei in Qinghai province, and standardized the collection of provincial geographic location data of animal plague surveillance (data not shown). In 2018, we also applied this system in Wulan County, which frequently experiences plague, and achieved a good application effect (data not shown).In the next step, we will expand the pilot areas (mainly national and provincial plague surveillance sites), collect surveillance data from each surveillance site, continuously optimize and update the system, improve the efficiency of data analysis and utilization, detect the plague epidemic in marmot in a timely and accurate manner, correctly determine the epidemic trend of plague in marmots, and attempt to strictly prevent the plague from spreading to humans. We plan to use a new model of drone surveillance to create a multidimensional, three-dimensional, real-time big data plague surveillance information reporting system to enhance early plague warnings and prediction in Qinghai province and even in the country, which will be of positive practical significance to serve and guarantee the Belt and Road Initiative. These approaches are expected to provide new technical means for plague investigation and research, and to provide references for setting up plague surveillance programs and prediction for the natural Himalayan marmot plague focus in Qinghai province and the QTP. More

Ren, W. et al. Changes of periphyton abundance and biomass driven by factors specific to flooding inflow in a river inlet area in Erhai Lake, China. Front. Environ. Sci. 9, 680718. https://doi.org/10.3389/fenvs.2021.680718 (2021).Article 

Google Scholar 
Woodruff, S. L. et al. The effects of a developing biofilm on chemical changes across the sediment-water interface in a freshwater environment. Int. Rev. Hydrobiol. 84(5), 509–532 (1999).CAS 

Google Scholar 
Muñoz, I., Real, M., Guasch, H., Navarro, E. & Sabater, S. Effects of atrazine on periphyton under grazing pressure. Aquat. Toxicol. 55(3–4), 239–249 (2001).
Google Scholar 
Hoagland, K. D., Roemer, S. C. & Rosowski, J. R. Colonization and community structure of two periphyton assemblages, with emphasis on the diatoms (Bacillariophyceae). Am. J. Bot. 69, 188–213. https://doi.org/10.2307/2443006 (1982).Article 

Google Scholar 
Steinman, A. D. & McIntire, C. D. Effects of current velocity and light energy on the structure of periphyton assemblages in laboratory streams. J. Phycol. 22, 352–361. https://doi.org/10.1111/J.1529-8817.1986.TB00035.X (1986).Article 

Google Scholar 
Tonkin, J. D., Death, R. G. & Barquín, J. Periphyton control on stream invertebrate diversity: Is periphyton architecture more important than biomass?. Mar. Freshw. Res. 65(9), 818–829 (2014).
Google Scholar 
Beck, W. S., Markman, D. W., Oleksy, I. A., Lafferty, M. H. & Poff, N. L. Seasonal shifts in the importance of bottom-up and top-down factors on stream periphyton community structure. Oikos 128, 680–691. https://doi.org/10.1111/oik.05844 (2018).Article 
CAS 

Google Scholar 
Hogsden, K. L. & Harding, J. S. Consequences of acid mine drainage for the structure and function of benthic stream communities: A review. Freshw. Sci. 31, 108–120. https://doi.org/10.1899/11-091.1 (2012).Article 

Google Scholar 
Sofi, M. S., Bhat, S. U., Rashid, I. & Kuniyal, J. C. The natural flow regime: A master variable for maintaining river ecosystem health. Ecohydrology 13(8), e2247. https://doi.org/10.1002/eco.2247 (2020).Article 

Google Scholar 
Biggs, B. J. F. Eutrophication of streams and rivers: Dissolved nutrient-chlorophyllrelationship for benthic algae. J. N. Am. Benthol. Soc. 19, 17–31 (2000).
Google Scholar 
Ormerod, S. J., Dobson, M., Hildrew, A. G. & Townsend, C. Multiple stressors in freshwater ecosystems. Freshw. Biol. 55, 1–4 (2010).
Google Scholar 
Poff, et al. The natural flow regime: A paradigm for river conservation and restoration. Bioscience 47, 769–784 (1997).
Google Scholar 
Naiman, R. J., Décamps, H., & McClain, M. E. Riparia: Ecology, Conservation and Management of Streamside Communities, (Elsevier/Academic Press, 2005).Gleick, P. H. Water use. Annu. Rev. Environ. Resour. 28, 275–314 (2003).
Google Scholar 
Jenkins, K. M. & Boulton, A. J. Connectivity in a dryland river: Short-term aquatic macroinvertebrate recruitment following floodplain inundation. Ecology 84(10), 2708–2723 (2003).
Google Scholar 
Biggs, B. J. F. Patterns in benthic algae of streams. In Algal Ecology in Freshwater Benthic Ecosystems (eds. Stevenson, R. J., Bothwell, M. L., & Lowe, R. L.) 31–56 (Academic Press, 1996).Smolar-Žvanut, N. & Mikoš, M. The impact of flow regulation by hydropower dams on the periphyton community in the Soča River, Slovenia. Hydrol. Sci. J. 59(5), 1032–1045. https://doi.org/10.1080/02626667.2013.834339 (2014).Article 
CAS 

Google Scholar 
Curry, C. J. & Baird, D. J. Habitat type and dispersal ability influence spatial structuring of larval Odonata and Trichoptera assemblages. Freshw. Biol. 60, 2142–2152 (2015).
Google Scholar 
Wu, N., Cai, Q. & Fohrer, N. Contribution of microspatial factors to benthic diatom communities. Hydrobiologia 732, 49–60. https://doi.org/10.1007/s10750-014-1843-3 (2014).Article 
CAS 

Google Scholar 
Mueller, M., Pander, J. & Geist, J. The effects of weirs on structural stream habitat and biological communities. J. Appl. Ecol 48(6), 1450–1461. https://doi.org/10.1111/j.1365-2664.2011.02035.x (2011).Article 

Google Scholar 
Davies, P. M. et al. Flow–ecology relationships: closing the loop on effective environmental flows. Mar. Freshw. Res. 65(2), 133–141 (2013).
Google Scholar 
Jun, Y. C. et al. Spatial distribution of benthic macroinvertebrate assemblages in relation to environmental variables in Korean nationwide streams. Water 8(1), 27. https://doi.org/10.3390/w8010027 (2016).Article 

Google Scholar 
Biggs, B. J. F. & Close, M. E. Periphyton biomass dynamics in gravel bed rivers: The relative effects of flows and nutrients. Freshw. Biol. 22, 209–231 (1989).CAS 

Google Scholar 
Jowett, I. & Biggs, B. J. F. Flood and velocity effects on periphyton and silt accumulation in two New Zealand rivers. N. Zeal. J. Mar. Freshw. Res. 31, 287–300 (1997).
Google Scholar 
Biggs, B. J. F., Goring, D. G. & Nikora, V. I. Subsidy and stress responses of stream periphyton to gradients in water velocity as a function of community growth form. J. Phycol. 34, 598–607 (1998).
Google Scholar 
Malmqvist, B. & Englund, G. Effects of hydropower-induced flow perturbations on mayfly (Ephemeroptera) richness and abundance in north Swedish river rapids. Hydrobiologia 341(2), 145–158 (1996).
Google Scholar 
Poff, N. L. & Ward, J. V. Herbivory under different flow regimes: A field experiment and test of a model with a benthic stream insect. Oikos 72, 179–188 (1995).
Google Scholar 
Poff, L. N., Wellnitz, T. & Monroe, J. B. Redundancy among three herbivorous insects across an experimental current velocity gradient. Oecologia 134, 262–269. https://doi.org/10.1007/s00442-002-1086-2 (2003).Article 

Google Scholar 
Vaughn, C. C. The role of periphyton abundance and quality in the microdistribution of a stream grazer, Helicopsyche borealis (Trichoptera: Helicopsychidae). Freshw. Biol. 16, 485–493 (1986).
Google Scholar 
Francoeur, S. N. Meta-analysis of lotic nutrient amendment experiments: Detecting and quantifying subtle responses. J. N. Am. Benthol. Soc. 20, 358–368 (2001).
Google Scholar 
Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).
Google Scholar 
Hillebrand, H. Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J. Phycol. 45, 798–806 (2009).
Google Scholar 
Lamberti, G. A. The role of periphyton in benthic food webs. In Algal Ecology—Freshwater Benthic Ecosystems, 533–572 (eds. Stevenson, R. J., Bothwell, M. L. & Lowe, R. L.) (Academic Press, 1996).Lamberti, G. A. et al. Influence of grazer type and abundance on plant–herbivore interactions in streams. Hydrobiologia 306, 179–188 (1995).
Google Scholar 
Gregory, S. V. Plant–herbivore interactions in stream systems. In Stream Ecology (eds. Barnes, J. R. & Minshall, G. W.) 157–189 (Plenum, 1983).Lamberti, G. A. & Moore, J. W. Aquatic insects as primary consumers. In The Ecology of Aquatic Insects (eds Resh, V. H. & Rosenberg, D. M.) 164–195 (Praeger, 1984).
Google Scholar 
Sterner, R. W., Elser, J. J. & Hessen, D. O. Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17, 49–67 (1992).CAS 

Google Scholar 
Kahlert, M. & Baunsgaard, M. T. Nutrient recycling—A strategy of a grazer community to overcome nutrient limitation. J. N. Am. Benthol. Soc. 18, 363–369 (1999).
Google Scholar 
Burkholder, J. M., Wetzel, R. G. & Klomparens, K. L. Direct comparison of phosphate uptake by adnate and loosely attached microalgae within and intact biofilm matrix. Appl. Environ. Microbiol. 56, 2882–2890 (1990).CAS 

Google Scholar 
Steinman, A. D. Effects of grazers on freshwater benthic algae. In Algal Ecology: Freshwater Benthic Ecosystems (eds. Stevenson, R. J., Bothwell & Lowe, R. L.) 341–366 (Academic Press, 1996).Smucker, N. J. & Vis, M. L. Spatial factors contribute to benthic diatom structure in streams across spatial scales: Considerations for biomonitoring. Ecol. Indic. 11, 1191–1203 (2011).
Google Scholar 
Myers, et al. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).Article 
CAS 

Google Scholar 
Wang, J., Pan, F., Soininen, J., Heino, J. & Shen, J. Nutrient enrichment modifies temperature-biodiversity relationship in large scale field experiments. Nat. Commun. 7, 13 (2016).
Google Scholar 
Wu, et al. Flow regimes filter species traits of benthic diatom communities and modify the functional features of lowland streams-a nationwide scale study. Sci. Total Environ. 651, 357–366 (2019).CAS 

Google Scholar 
Nisar, M. A. Geospatial approach to study environmental characterization of a Kashmir wetland (Anchar) catchment with special reference to land use/land cover and changing climate. Ph.D Thesis, Sher-e-Kashmir University of Agricultural Sciences and Technology, Kashmir. Weblink. http://krishikosh.egranth.ac.in/handle/1/91309 (2012).Bhat, S. U., Sofi, A. H., Yaseen, T., Pandit, A. K. & Yousuf, A. R. Macro invertebrate community from Sonamarg streams of Kashmir Himalaya. Pak. J. Biol. Sci. 14(3), 182–194. https://doi.org/10.3923/pjbs.2011.182.194 (2011).Article 
CAS 

Google Scholar 
Baba, A. I., Sofi, A. H., Bhat, S. U., & Pandit, A. K. Periphytic algae of river Sindh in the Sonamarg area of Kashmir valley. J. Phytol. 3(6) (2011).Sofi, M. S., Rautela, K. S., Bhat, S. U., Rashid, I. & Kuniyal, J. C. Application of geomorphometric approach for the estimation of hydro-sedimentological flows and cation weathering rate: Towards understanding the sustainable land use policy for the Sindh Basin, Kashmir Himalaya. Water Air Soil Pollut. 232(7), 1–11. https://doi.org/10.1007/s11270-021-05217-w (2021).Article 
CAS 

Google Scholar 
Romshoo, S. A., & Fayaz, M. Use of high resolution remote sensing for improving environmental Friendly tourism master planning in the Alpine Himalaya: A case study of Sonamarg tourist resort, Kashmir. J. Himalayan Ecol. Sustain. Dev. 14 (2019).Biggs, B. J. F. & Kilroy, C. Stream periphyton monitoring manual. Published by NIWA for Ministry for the Environment, 226 Christchurch, New Zealand: NIWA (2000).APHA. Standard Methods for Examination of Water and Wastewater, 22nd edn. (American Public Health Association, 2012).Cox, E. J. Identification of Freshwater Diatoms from Live Material. (Chapman and Hall, 1996). https://doi.org/10.1017/S0025315400041023.Krammer, K., & Lange-Bertalot, H. Bacillariophyceae, Part 5. English and French Translation of the Keys. (VEB Gustav Fisher Verlag, 2000).Reichardt, E. A remarkable association of diatoms in a spring habitat in the Grazer Bergland, Austria. In Iconographia Diatomologica (ed. Lange-Bertalot, H.) 419–479 (2004).Żelazna-Wieczorek, J. Diatom flora in springs of Lódz Hills (Central Poland). Biodiversity, taxonomy and temporal changes of epipsammic diatom assemblages in springs affected by human impact, 419. Volume 13 of Diatom monographs. Gantner. https://books.google.co.in/books?id=bdxeewAACAAJ (2011).Stark, J. D., Boothroyd, I. K. G., Harding, J. S., Maxted, J. R. & Scarsbrook, M. R. Protocols for sampling macroinvertebrates in wadeable streams. In New Zealand Macroinvertebrate Working Group Report no. 1. Prepared for the Ministry for the Environment. Sustainable Management Fund Project, 5103 (2001).Winterbourn, M. J. Sampling stream invertebrates. In Biological Monitoring of Freshwaters. Proceedings of the Seminar. Water and Soil Miscellaneous Publication No. 83 (eds. Pridmore, R. D., Cooper, A. B.) 241–258. (National Water and Soil Conservation Authority, 1985).Barbour, M. T., Gerritsen, J., Snyder, B. D., Stribling, J. B. Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish, 339. (United States Environmental Protection Agency, Office of Water, 1999).Malmqvist, B. & Hoffsten, P. O. Macroinvertebrate taxonomic richness, community structure and nestedness in Swedish streams. Fundam. Appl. Limnol. 150(1), 29–54. https://doi.org/10.1127/archiv-hydrobiol/150/2000/29 (2000).Article 

Google Scholar 
Ilmonen, J. & Paasivirta, L. Benthic macrocrustacean and insect assemblages in relation to spring habitat characteristics: Patterns in abundance and diversity. Hydrobiologia 533(1–3), 99–113. https://doi.org/10.1007/s10750-004-2399-4 (2005).Article 

Google Scholar 
Munasinghe, D. S. N., Najim, M. M. M., Quadroni, S. & Musthafa, M. M. Impacts of streamflow alteration on benthic macroinvertebrates by mini-hydro diversion in Sri Lanka. Sci. Rep. 11(1), 546. https://doi.org/10.1038/s41598-020-79576-5 (2021).Article 
CAS 

Google Scholar 
Edmondson, W. T. Fresh-Water Biology, 2nd ed. 1050–1056 (Wiley, 1959).Pennak, R. W. Freshwater Invertebrates of United States. (Wiley, 1978).McCafferty, W. P., Provonsha, A. V. Aquatic entomology: The fishermen’s and ecologists’ Illustrated Guide to Insects and their Relatives. (Jones and Bartlett Publishers, 1983).Borror, D., Triplehorn, C., Johnson, N. An Introduction to the Study of Insects, 6th ed. (Saunders College Publishing, 1989).Ward, J. V. Aquatic Insect Ecology, Biology and Habitat. (Wiley, 1992).Engblom, E. & Lingdell, P.E. Analyses of Benthic Invertebrates (ed. Nyman, L.) (1999).Bouchard, R. W. Guide to Aquatic Invertebrates of the Upper Midwest: Identification Manual for Students (University of Minnesota, 2004).
Google Scholar 
Subramanian, K. A. & Sivaramakrishnan, K. G. Aquatic Insects for Biomonitoring Freshwater Ecosystems—A Methodology Manual. (Ashoka Trust for Ecology and Environment (ATREE), 2007).Thorp, J. H., & Covich, A. P. (eds.) Ecology and Classification of North American Freshwater Invertebrates. (Academic Press, 2009).Allan, J. D. & Castillo, M.M. An introduction to fluvial ecosystems. In Stream Ecology: Structure and Function of Running Waters, 1–12 (2007).Oksanen, et al. Vegan: Community ecology package. In: R package version 2.4-3.McCune, B. & Grace, B. Analysis of Ecological Communities (MjM Software Design, 2016).Clarke, K. R. & Gorley, R. N. Primer v6 Permanova+ (Primer-E Ltd., 2006).
Google Scholar 
Salazar, G. EcolUtils: Utilities for Community Ecology Analysis. R package version 0.1 software (2018).Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9(6), 683–693 (2006).
Google Scholar 
Gardener, M. Community Ecology: Analytical Methods in Using R and Excel. (Pelagic Publishing, 2014).Chao, A. & Bunge, J. Estimating the number of species in a stochastic abundance model. Biometrics 58, 531–539. https://doi.org/10.1111/j.0006-341X.2002.00531.x (2002).Article 
MATH 

Google Scholar 
Peres-Neto, P. R., Legendre, P., Dray, S. & Borcard, D. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 2614–2625 (2006).
Google Scholar 
Meng, X. L. et al. Responses of macroinvertebrates and local environment to short-term commercial sand dredging practices in a flood-plain lake. Sci. Total Environ. 631, 1350–1359 (2018).
Google Scholar 
Core Team, R. R: A Language and Environmental for Statistical Computing. (R Foundation for Statistical Computing, 2017).Wood, P. J. & Armitage, P. D. Biological effects of fine sediment in the lotic environment. Environ. Manag. 21, 203–217 (1997).CAS 

Google Scholar 
Marchant, R. Changes in the benthic invertebrate communities of the Thomson River, southeastern Australia, after dam construction. Regul. Rivers Res. Manag. 4, 71–89 (1989).
Google Scholar 
Gray, L. J. & Ward, J. V. Effects of sediment releases from a reservoir on stream macroinvertebrates. Hydrobiologia 96, 177–184 (1982).
Google Scholar 
Sand-Jensen, K., Moller, J. & Olesen, B. H. Biomass regulation of microbenthic algae in Danish lowland streams. Oikos 53, 332–340 (1988).
Google Scholar 
Lewis, M. A., Weber, D. E., Stanley, R. S. & Moore, J. C. Dredging impact on an urbanized Florida bayou: Effects on benthos and algal-periphyton. Environ. Pollut. 115(2), 161–171 (2001).CAS 

Google Scholar 
Biggs, B. J. Algal ecology in freshwater benthic ecosystems geology and landuse to the habitat template of periphyton in stream ecosystems. Freshw. Biol. 33, 419–438 (1995).
Google Scholar 
Taylor, et al. Can diatom-based pollution indices be used for biomonitoring in South Africa? A case study of the Crocodile West and Marico water management area. Hydrobiologia 592, 455–464 (2007).
Google Scholar 
Porter, et al. Efficacy of algal metrics for assessing nutrient and organic enrichment in flowing waters. Freshw. Biol. 53, 1036–1054 (2008).
Google Scholar 
Wetzel, R. G. & Likens, G. E. Limnological analyses, 3rd ed. In Nitrogen, Phosphorus, and Other Nutrients, 85–113. (Springer, 2000). https://doi.org/10.1007/978-1-4757-3250-4.Wetzel, R. G. Attached algal-substrata interactions: Fact or myth, and when and how? vol. 17. In Periphyton of Freshwater Ecosystems (ed. Wetzel, R.) 207–215 (Springer, 1983). https://doi.org/10.1007/978-94-009-7293-3_28.Krajenbrink, H. J. et al. Diatoms as indicators of the effects of river impoundment at multiple spatial scales. PeerJ 7, e8092. https://doi.org/10.7717/peerj.8092 (2019).Article 

Google Scholar 
Poff, N. L., Voelz, N. J., Ward, J. V. & Lee, R. E. Algal colonization under four experimentally-controlled current regimes in a high mountain stream. J. N. Am. Benthol. Soc. 9, 303–318 (1990).
Google Scholar 
Dodds, W. K. & Marra, J. L. Behaviors of the midge, Cricotopus (Diptera; Chironomidae) related to mutualism with Nostoc parmeloides (Cyanobacteria). Aquat. Insects 11, 201–208 (1989).
Google Scholar 
Tang, T., Niu, S. Q. & Dudgeon, D. Responses of epibenthic algal assemblages to water abstraction in Hong Kong streams. Hydrobiologia 703(1), 225–237. https://doi.org/10.1007/s10750-012-1362-z (2013).Article 
CAS 

Google Scholar 
Maheshwari, K., Vashistha, J., Paulose, P. V. & Agarwal, T. Seasonal changes in phytoplankton community of lake Ramgarh, India. Int. J. Curr. Microbiol. Appl. Sci. 4(11), 318–330 (2015).CAS 

Google Scholar 
Luttenton, M. R., & Baisden, C. The relationships among disturbance, substratum size and periphyton community structure. In Advances in Algal Biology: A Commemoration of the Work of Rex Lowe 111–117. (Springer, 2006).Uehlinger, U. Spatial and temporal variability of periphyton biomass in a prealpine river (Necker, Switzerland). Arch. Fur. Hydrobiol. 123, 219–237 (1991).
Google Scholar 
Hill, W. R. Effects of light. In Algal Ecology in Freshwater Benthic Ecosystems. 121–148 (eds. Stevenson, R. J., Bothwell, M. L., Lowe, R. L.) (Academic Press, 1996).DeNichola, D. M. Periphyton responses to temperature at different ecological levels. In Algal Ecology in Freshwater Benthic Ecosystems. (eds. Stevenson, R. J., Bothwell, M. L., Lowe, R. L.) 149–181 (Academic Press, 1996).O’Reilly, C. M. Seasonal dynamics of periphyton in a large tropical lake. Hydrobiologia 553, 293–301. https://doi.org/10.1007/s10750-005-0878-x (2006).Article 

Google Scholar 
Borduqui, M. & Ferragut, C. Factors determining periphytic algae succession in a tropical hypereutrophic reservoir. Hydrobiologia 683, 109–122. https://doi.org/10.1007/s10750-011-0943-6 (2012).Article 
CAS 

Google Scholar 
De Souza, M. L., Pellegrini, B. G. & Ferragut, C. Periphytic algal community structure in relation to seasonal variation and macrophyte richness in a shallow tropical reservoir. Hydrobiologia 755, 183–196. https://doi.org/10.1007/s10750-015-2232-2 (2015).Article 

Google Scholar 
Prowse, T. D. River-ice hydrology. In Encyclopedia of Hydrological Sciences, vol. 4 (ed. Anderson, M. G.). (Wiley, 2005).Rusanov, A. G., Stanislavskaya, E. V. & Ács, É. Periphytic algal assemblages along environmental gradients in the rivers of the Lake Ladoga basin, Northwestern Russia: Implication for the water quality assessment. Hydrobiologia 695(1), 305–327 (2012).CAS 

Google Scholar 
Sofi, M. S., Hamid, A., Bhat, S. U., Rashid, I. & Kuniyal, J. C. Impact evaluation of the run-of-river hydropower projects on the water quality dynamics of the Sindh River in the Northwestern Himalayas. Environ. Monit. Assess. 194(9), 1–6 (2022).
Google Scholar 
MCCormick, P. V. Resource competition and species coexistence in freshwater algal assemblages. In Algal ecology—Freshwater Benthic Ecosystems (eds. Stevenson, R. J., Bothwell, M. L., Lowe, R. L.) 229–252 (Academic, 1996).Hillebrand, H., Worm, B. & Lotze, H. K. Marine microbenthic community structure regulated by nitrogen loading and grazing pressure. Mar. Ecol. Prog. Ser. 204, 27–38 (2000).CAS 

Google Scholar  More

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

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

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