Philippa Kaur

Alexander, R. D., Marshall, D. C. & Cooley, J. R. in The Evolution of Mating Systems in Insects and Arachnids (eds. Choe, J. C. & Crespi, B. J.) 4–31 (Cambridge Univ. Press, 1997).Clements, A. N. The Biology of Mosquitoes. Volume 2: Sensory, Reception and Behaviour (CABI Publishing, 1999).Downes, J. A. The swarming and mating flight of Diptera. Annu. Rev. Entomol. 14, 271–298 (1969).Article 

Google Scholar 
Gibson, N. H. E. On the mating swarms of certain Chironomidae (Diptera). Trans. R. Entomol. Soc. Lond. 95, 263–294 (1945).Article 

Google Scholar 
Sivinski, J. M. & Petersson, E. in The Evolution of Mating Systems in Insects and Arachnids (eds. Choe, J. A. & Crespi, J. B.) 294–309 (Cambridge Univ. Press, 1997).Shelly, T. E. & Whittier, T. S. in The Evolution of Mating Systems in Insects and Arachnids (eds. Choe, J. A. & Crespi, J. B.) 273–293 (Cambridge Univ. Press, 1997).Savolainen, E. Swarming in Ephemeroptera: the mechanism of swarming and the effects of illumination and weather. Ann. Zool. Fennici 15, 17–52 (1978).
Google Scholar 
Howell, P. I. & Knols, B. G. J. J. Male mating biology. Malar. J. 8, S8 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Charlwood, J. D. & Jones, M. D. R. Mating in the mosquito, Anopheles gambiae s.l. II. Swarming behaviour. Physiol. Entomol. 5, 315–320 (1980).Article 

Google Scholar 
Marchand, R. P. Field observations on swarming and mating in Anopheles gambiae mosquitoes in Tanzania. Neth. J. Zool. 34, 367–387 (1984).Article 

Google Scholar 
Charlwood, J. D. et al. The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera: Culicidae) from São Tomé Island. J. Vector Ecol. 27, 178–183 (2002).CAS 
PubMed 

Google Scholar 
Diabaté, A. et al. Natural swarming behaviour of the molecular M form of Anopheles gambiae. Trans. R. Soc. Trop. Med. Hyg. 97, 713–716 (2003).Article 
PubMed 

Google Scholar 
Diabaté, A. et al. Spatial swarm segregation and reproductive isolation between the molecular forms of Anopheles gambiae. Proc. R. Soc. B Biol. Sci. 276, 4215–4222 (2009).Article 

Google Scholar 
Sawadogo, P. S. et al. Swarming behaviour in natural populations of Anopheles gambiae and An. coluzzii: review of 4 years survey in rural areas of sympatry, Burkina Faso (West Africa). Acta Trop. 130, 24–34 (2014).Article 

Google Scholar 
della Torre, A. et al. Molecular evidence of incipient speciation within Anopheles gambiae s.s. in West Africa. Insect Mol. Biol. 10, 9–18 (2001).Article 
PubMed 

Google Scholar 
della Torre, A., Tu, Z. & Petrarca, V. On the distribution and genetic differentiation of Anopheles gambiae s.s. molecular forms. Insect Biochem. Mol. Biol. 35, 755–769 (2005).Article 
CAS 
PubMed 

Google Scholar 
Tripet, F. et al. DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol. Ecol. 10, 1725–1732 (2001).CAS 
Article 
PubMed 

Google Scholar 
Diabaté, A. et al. Mixed swarms of the molecular M and S forms of Anopheles gambiae (Diptera: Culicidae) in sympatric area from Burkina Faso. J. Med. Entomol. 43, 480–483 (2006).Article 
PubMed 

Google Scholar 
Costantini, C. et al. Living at the edge: biogeographic patterns of habitat segregation conform to speciation by niche expansion in Anopheles gambiae. BMC Ecol. 9, 16 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sawadogo, P. S. et al. Differences in timing of mating swarms in sympatric populations of Anopheles coluzzii and Anopheles gambiae s.s. (formerly An. gambiae M and S molecular forms) in Burkina Faso, West Africa. Parasit. Vectors 6, 275 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Persiani, A., Dideco, M. A. & Petrangeli, G. Osservzioni di laboratorio su polimorfismi da inversione originati da incroci tra popolazioni diverse di Anopheles gambiae s.s. Ann. Dell’Istituto Super. Di Sanita 22, 221–224 (1986).CAS 

Google Scholar 
Diabaté, A. et al. Larval development of the molecular forms of Anopheles gambiae (Diptera: Culicidae) in different habitats: a transplantation experiment. J. Med. Entomol. 42, 548–553 (2005).Article 
PubMed 

Google Scholar 
Diabaté, A., Dabiré, K. R., Millogo, N. & Lehmann, T. Evaluating the effect of postmating isolation between molecular forms of Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 44, 60–64 (2007).Article 
PubMed 

Google Scholar 
Hahn, M. W., White, B. J., Muir, C. D. & Besansky, N. J. No evidence for biased co-transmission of speciation Islands in Anopheles gambiae. Philos. Trans. R. Soc. B Biol. Sci. 367, 374–384 (2012).Article 

Google Scholar 
Pombi, M. et al. Dissecting functional components of reproductive isolation among closely related sympatric species of the Anopheles gambiae complex. Evol. Appl. 00, 1–19 (2017).
Google Scholar 
Lehmann, T. & Diabaté, A. The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect. Genet. Evol. 8, 737–746 (2008).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Clements, A. N. The Biology of Mosquitoes: Development, Nutrition and Reproduction (Chapman & Hall, 1992).Gibson, G., Warren, B. & Russell, I. J. Humming in tune: sex and species recognition by mosquitoes on the wing. J. Assoc. Res. Otolaryngol. 11, 527–540 (2010).Article 
PubMed 
PubMed Central 

Google Scholar 
Pennetier, C., Warren, B., Dabiré, K. R., Russell, I. J. & Gibson, G. ‘Singing on the wing’ as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr. Biol. 20, 131–136 (2010).CAS 
Article 
PubMed 

Google Scholar 
Feugère, L., Gibson, G., Manoukis, N. C. & Roux, O. Mosquito sound communication: are male swarms loud enough to attract females? J. R. Soc. Interface 18, 20210121 (2021).Article 
PubMed 
PubMed Central 

Google Scholar 
Poda, S. B. et al. Sex aggregation and species segregation cues in swarming mosquitoes: role of ground visual markers. Parasit. Vectors 12, 589 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Wang, G. et al. Clock genes and environmental cues coordinate Anopheles pheromone synthesis, swarming, and mating. Science 371, 411–415 (2021).CAS 
Article 
PubMed 

Google Scholar 
Dao, A. et al. Assessment of alternative mating strategies in Anopheles gambiae: does mating occur indoors? J. Med. Entomol. 45, 643–652 (2008).PubMed 

Google Scholar 
Gomulski, L. Aspects of Mosquito Mating Behaviour. PhD thesis, Univ. London (1988).Kelly, D. W. & Dye, C. Pheromones, kairomones and the aggregation dynamics of the sandfly Lutzomyia longipalpis. Anim. Behav. 53, 721–731 (1997).Article 

Google Scholar 
Bray, D. P., Alves, G. B., Dorval, M. E., Brazil, R. P. & Hamilton, J. G. C. Synthetic sex pheromone attracts the leishmaniasis vector Lutzomyia longipalpis to experimental chicken sheds treated with insecticide. Parasit. Vectors 3, 16 (2010).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Diabaté, A. et al. Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evol. Biol. 11, 184 (2011).Article 
PubMed 
PubMed Central 

Google Scholar 
Levi-Zada, A. et al. Diel periodicity of pheromone release by females of Planococcus citri and Planococcus ficus and the temporal flight activity of their conspecific males. Naturwissenschaften 101, 671–678 (2014).CAS 
Article 
PubMed 

Google Scholar 
Bjostad, L. B., Gaston, L. K. & Shorey, H. H. Temporal pattern of sex pheromone release by female Trichoplusia ni. J. Insect Physiol. 26, 493–498 (1980).Article 

Google Scholar 
Merlin, C. et al. An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J. Biol. Rhythms 22, 502–514 (2007).CAS 
Article 
PubMed 

Google Scholar 
Rund, S. S. C. et al. Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae. Sci. Rep. 3, 2494 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Robledo, N. & Arzuffi, R. Influence of host fruit and conspecifics on the release of the sex pheromone by Toxotrypana curvicauda males (Diptera: Tephritidae). Environ. Entomol. 41, 387–391 (2012).CAS 
Article 
PubMed 

Google Scholar 
Andersson, J. et al. Male sex pheromone release and female mate choice in a butterfly. J. Exp. Biol. 210, 964–970 (2007).CAS 
Article 
PubMed 

Google Scholar 
Mozūraitis, R. et al. Male swarming aggregation pheromones increase female attraction and mating success among multiple African malaria vector mosquito species. Nat. Ecol. Evol. 4, 1395–1401 (2020).Article 
PubMed 

Google Scholar 
Poda, S. B. et al. No evidence for long-range male sex pheromones in two malaria mosquitoes. Preprint at bioRxiv https://doi.org/10.1101/2020.07.05.187542 (2021).Verhulst, N. O. et al. Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLoS ONE 5, e15829 (2010).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Pandey, S. K. & Kim, K. Human body-odor components and their determination. Trends Anal. Chem. 30, 784–796 (2011).CAS 
Article 

Google Scholar 
Dormont, L., Bessiere, J. M., McKey, D. & Cohuet, A. New methods for field collection of human skin volatiles and perspectives for their application in the chemical ecology of human-pathogen-vector interactions. J. Exp. Biol. 216, 2783–2788 (2013).CAS 
PubMed 

Google Scholar 
Dormont, L., Bessière, J. M. & Cohuet, A. Human skin volatiles: a review. J. Chem. Ecol. 39, 569–578 (2013).CAS 
Article 
PubMed 

Google Scholar 
Tchouassi, D. P. et al. Common host-derived chemicals increase catches of disease-transmitting mosquitoes and can improve early warning systems for rift valley fever virus. PLoS Negl. Trop. Dis. 7, e2007 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
McBride, C. S. et al. Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515, 222–227 (2014).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Poli, D. et al. Determination of aldehydes in exhaled breath of patients with lung cancer by means of on-fiber-derivatisation SPME-GC/MS. J. Chromatogr. B. 878, 2643–2651 (2010).CAS 
Article 

Google Scholar 
Filipiak, W. et al. Comparative analyses of volatile organic compounds (VOCs) from patients, tumors and transformed cell lines for the validation of lung cancer-derived breath markers. J. Breath. Res. 8, 027111 (2014).CAS 
Article 
PubMed 

Google Scholar 
Calenic, B. & Amann, A. Detection of volatile malodorous compounds in breath: current analytical techniques and implications in human disease. Bioanalysis 6, 357–376 (2014).CAS 
Article 
PubMed 

Google Scholar 
Cainap, C., Pop, L. A., Balacescu, O. & Cainap, S. S. Early diagnosis and screening in lung cancer. Am. J. Cancer Res. 10, 1993–2009 (2020).CAS 
PubMed 
PubMed Central 

Google Scholar 
Dekel, A., Yakir, E. & Bohbot, J. D. The sulcatone receptor of the strict nectar-feeding mosquito Toxorhynchites amboinensis. Insect Biochem. Mol. Biol. 111, 103174 (2019).CAS 
Article 
PubMed 

Google Scholar 
Nyasembe, V. O. et al. Development and assessment of plant-based synthetic odor baits for surveillance and control of malaria vectors. PLoS Negl. Trop. Dis. 9, e89818 (2014).
Google Scholar 
Wondwosen, B. et al. Sweet attraction: sugarcane pollen-associated volatiles attract gravid Anopheles arabiensis. Malar. J. 17, 90 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wondwosen, B. et al. Rice volatiles lure gravid malaria mosquitoes, Anopheles arabiensis. Sci. Rep. 6, 37930 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Suh, E., Choe, D., Saveer, A. M. & Zwiebel, L. J. Suboptimal larval habitats modulate oviposition of the malaria vector mosquito Anopheles coluzzii. PLoS ONE 11, e0149800 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kostiainen, R. Volatile organic compounds in the indoor air of normal and sick houses. Atmos. Environ. 29, 693–702 (1995).CAS 
Article 

Google Scholar 
Kruza, M., Lewis, A. C., Morrison, C. G. & Carslaw, N. Impact of surface ozone interactions on indoor air chemistry: a modeling study. Indoor Air 27, 1001–1011 (2017).CAS 
Article 
PubMed 

Google Scholar 
Tripet, F., Dolo, G., Traoré, S. & Lanzaro, G. C. The ‘wingbeat hypothesis’ of reproductive isolation between members of the Anopheles gambiae complex (Diptera: Culicidae) does not fly. J. Med. Entomol. 41, 375–384 (2004).Article 
PubMed 

Google Scholar 
Facchinelli, L. et al. Stimulating Anopheles gambiae swarms in the laboratory: application for behavioural and fitness studies. Malar. J. 14, 271 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Niang, A. et al. Semi-field and indoor setups to study malaria mosquito swarming behavior. Parasit. Vectors 12, 446 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Gibson, G. Swarming behaviour of the mosquito Culex pipiens quinquefasciatus: a quantitative analysis. Physiol. Entomol. 10, 283–296 (1985).Article 

Google Scholar 
Bimbilé Somda, N. S. et al. Ecology of reproduction of Anopheles arabiensis in an urban area of Bobo-Dioulasso, Burkina Faso (West Africa): monthly swarming and mating frequency and their relation to environmental factors. PLoS ONE 13, e0205966 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Maïga, H., Dabiré, R. K., Lehmann, T., Tripet, F. & Diabaté, A. Variation in energy reserves and role of body size in the mating system of Anopheles gambiae. J. Vector Ecol. 37, 289–297 (2012).Article 
PubMed 

Google Scholar 
Maïga, H. et al. Role of nutritional reserves and body size in Anopheles gambiae males mating success. Acta Trop. 132S, S102–S107 (2014).Article 

Google Scholar 
Schiestl, F. P. The evolution of floral scent and insect chemical communication. Ecol. Lett. 13, 643–656 (2010).Article 
PubMed 

Google Scholar 
Goodrich, K. R., Zjhra, M. L., Ley, C. A. & Raguso, R. A. When flowers smell fermented: the chemistry and ontogeny of yeasty floral scent in Pawpaw (Asimina triloba: Annonaceae). Int. J. Plant Sci. 167, 33–46 (2006).CAS 
Article 

Google Scholar 
Iatrou, K. & Biessmann, H. Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem. Mol. Biol. 38, 268–274 (2008).CAS 
Article 
PubMed 

Google Scholar 
Pitts, R. J., Rinker, D. C., Jones, P. L., Rokas, A. & Zwiebel, L. J. Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 12, 271 (2011).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Lu, T. et al. Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr. Biol. 17, 1533–1544 (2007).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Guidobaldi, F., May-Concha, I. J. & Guerenstein, P. G. Morphology and physiology of the olfactory system of blood-feeding insects. J. Physiol. Paris 108, 96–111 (2014).CAS 
Article 
PubMed 

Google Scholar 
Mosqueira, B. et al. Pilot study on the combination of an organophosphate-based insecticide paint and pyrethroid-treated long lasting nets against pyrethroid resistant malaria vectors in Burkina Faso. Acta Trop. 148, 162–169 (2015).CAS 
Article 
PubMed 

Google Scholar 
Poda, S. B. et al. Targeted application of an organophosphate-based paint applied on windows and doors against Anopheles coluzzii resistant to pyrethroids under real life conditions in Vallée du Kou, Burkina Faso (West Africa). Malar. J. 17, 136 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Diabaté, A. et al. The spread of the Leu-Phe kdr mutation through Anopheles gambiae complex in Burkina Faso: genetic introgression and de novo phenomena. Trop. Med. Int. Heal. 9, 1267–1273 (2004).Article 

Google Scholar 
Santolamazza, F. et al. Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms. Malar. J. 7, 163 (2008).Article 
PubMed 
PubMed Central 

Google Scholar 
Lefèvre, T. et al. Evolutionary lability of odour-mediated host preference by the malaria vector Anopheles gambiae. Trop. Med. Int. Heal. 14, 228–236 (2009).Article 

Google Scholar 
Lefèvre, T. et al. Beer consumption increases human attractiveness to malaria mosquitoes. PLoS ONE 5, e9546 (2010).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Vantaux, A. et al. Host-seeking behaviors of mosquitoes experimentally infected with sympatric field isolates of the human malaria parasite Plasmodium falciparum: no evidence for host manipulation. Front. Ecol. Evol. 3, 86 (2015).Article 

Google Scholar 
Nguyen, P. L. et al. No evidence for manipulation of Anopheles gambiae, An. coluzzii and An. arabiensis host preference by Plasmodium falciparum. Sci. Rep. 7, 9415 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Tienpont, B., David, F., Bicchi, C. & Sandra, P. High capacity headspace sorptive extraction. J. Microcolumn Sep. 12, 577–584 (2000).CAS 
Article 

Google Scholar 
Bicchi, C., Cordero, C., Iori, C., Rubiolo, P. & Sandra, P. Headspace Sorptive Extraction (HSSE) in the headspace analysis of aromatic and medicinal plants. J. High. Resolut. Chromatogr. 23, 539–546 (2000).CAS 
Article 

Google Scholar 
Souto-Vilarós, D. et al. Pollination along an elevational gradient mediated both by floral scent and pollinator compatibility in the fig and fig-wasp mutualism. J. Ecol. 106, 2256–2273 (2018).Article 

Google Scholar 
Zellner, Bd’Acampora et al. Linear retention indices in gas chromatographic analysis: a review. Flavour Fragr. J. 23, 297–314 (2008).Article 
CAS 

Google Scholar 
Charpentier, M. J. E., Barthes, N., Proffit, M., Bessière, J. M. & Grison, C. Critical thinking in the chemical ecology of mammalian communication: roadmap for future studies. Funct. Ecol. 26, 769–774 (2012).Article 

Google Scholar  More

Sewage and TSE quantity characteristicsThe WWT facilities have been implemented for Zabol with a capacity of 39,000 m3/day. Table 1 shows the volume of water consumption and sewage production based on the sewage coefficient in urban communities of the study area.Table 1 Water consumption, TSE volume and receiving resources in the study area—2019.Full size tableAs shown in Table 1, the total water consumption in the study area is 22.538 mcm/year while based on the development conditions. Afterward, the sewage volume was calculated to 16.194 mcm/year, considering the sewage coefficient and water consumption.Continuously, the sewage data obtained from the Water and Wastewater Organization of Zabol city, Iran, showed that the sewage entrance to the treatment plants of the study area is about 19,000 m3/day and 137 working days. Therefore, the TSE volume of the WWT plant was calculated based on the following scenarios of (1) data obtained from the Water and Wastewater Organization, Iran, and (2) based on the capacity of WWT plant. Note that the working days for both scenarios will be 137. The calculation is based on Eq. (1). The total TSE volume for scenarios 1 and 2 is 2.8 and 5.1 mcm/year, respectively.The difference between the calculation based on capacity and the existing data is due to the removal of raw sewage before entering the treatment plant, which has caused health and environmental problems in the region. Data obtained from Iran Department of Environment34 showed that 1.68 mcm/y of sewage were extracted for the farms. Previous studies in the same study area also reported the significant (P  5. Note that typical abundance of total and fecal coliforms (FC) in raw sewage are 107–109 and 106–108 100/mL, respectively, and were reduced by 1–5 orders of magnitude in treated TSE, depending on the type of treatment39,40. Classical treatments, which do not include any specific disinfection step, reduce fecal micro-organisms densities by 1–3 orders of magnitude40, but because of their high abundance in raw sewage, they are still discharged in large numbers with treated TSEs in the environment.Figure 6The results of the abundance of total coliforms (TC) and fecal coliforms (FC).Full size imageAdditionally, the results of yearly values of physicochemical factors of Zabol TSE (mg/L) including BOD5, COD, TDS, TH, and EC in the period of 2017–2019, showed in Fig. 7. The yearly results suggested that the values through the years of investigation did not show significant changes. In the following parts, the possibility of TSE evaluated considering various standards.Figure 7The results of yearly values of physicochemical factors of Zabol TSE.Full size imagePotential application of TSEComparing the quality of the TSE and sewage are based on various regulations showed in Table 3. It includes the food and agriculture organization (FAO), US environmental protection agency (USEPA), the Canadian water quality index (CWQI), and Iran’s national standards (INS), considering the irrigation and recreational application.Table 3 Guidelines for interpretations of water quality of sewage and TSE of Zabol WWT plants (average in the period of 2017–2019) compared to the standards of regulations.Full size tableAccording to the FAO Guide41 for Classifying Agricultural Water Quality, as shown in Table 3, the most crucial parameters for the application of TSE in irrigation include electrical conductivity (EC), sodium uptake ratio (SAR), chlorine, BOD, COD, and FC. However, three out of seven parameters namely BOD, COD, and FC in the TSE are largely erratic with the limits recommended in the standards.Based on USEPA42, the value of total suspended solids in TSE of Zabol WWT plant largely inconsistent with the limits recommended in the standards for TSE reuse. However, TDS, EC, and pH, met the criteria. Moreover, except TSS and pH, the other chemical parameters of sewage also meet the criteria. It is worth mentioning that EPA does not require or restrict any types of water reuse. Generally, states maintain primary regulatory authority (i.e., primacy) in allocating and developing water resources. Some US states have established programs to specifically address reuse, and some have incorporated water reuse into their existing programs. EPA, states, tribes, and local governments implement programs under the Safe Drinking Water Act and the Clean Water Act to protect the quality of drinking water source waters, community drinking water, and waterbodies like rivers and lakes.According to INS regulations for irrigation and recreation reuse of TSE33, the value parameters tested for the TSE of the Zabol WWT plant are following the limits recommended in the standards for consumption as irrigation (except chlorine) and recreation projects.Finally, the CWQI is a means to provide consistent procedures for Canadian jurisdictions to report water quality information to both management and the public. The CWQI value ranges between 1 and 100, and the result is further simplified by assigning it to a descriptive category in Table 4.Table 4 The CWQI value and descriptive.Full size tableThe results of CWQI software for analyzing the TSE of the WWT plant in the study area, as shown in Table 5 and Fig. 8, indicated its poor quality for drinking, and aquatic. While it is fair for livestock and marginal for irrigation. However, considering the purpose of this study for irrigation of the native plants, it met the criteria. Note that the input data set is based on the period of 2017–2019.Table 5 The results of TSE in various applications assessed by CWQI.Full size tableFigure 8CWQI tets results for TSE of WWT plant in the study area.Full size imageThe results of this section indicated the consideration of various parameters due to various regulations and demonstrated that the treatment technology upgrade was significantly better than those of urban miscellaneous water and agriculture water standards, indicating this system can be widely used for urban landscape hydration. Moreover, squeezing the sewage treatment process for being cost effective could be recommended considering the measurements of FC, BOD, and COD.Optimal area suggestion for project executionConsidering three steps of wind erosion which are detachment, transportation, and deposition, the sand fixation methods have to be done in the detachment area to be more effective. Hence, the most advantageous regions for project execution were selected based on the factors of (a) discovering the dust origins, and (b) vegetation cover. Regarding the first concern, it was shown that the dry sediments of the Farah river43, and the presence of dunes between the two sand movements corridors in Sistan, namely Jazinak (near Zabol city) and Tasuki corridors (shown in Fig. 9), was increased the dust concentration in Zabol city37,44 while the agricultural lands, and other infrastructures such as roads, and irrigation canals developed in the area between Zahedan and Zabol city.Figure 9Locations and names of Hamuns lake and sand movement corridors in the study area © 2022 by Springer Nature Limited is licensed under Attribution 4.0 International (created by ArcMap 10.5).Full size imageSubsequently, based on a guide that 30% of vegetation cover has a significant effect on the process of soil detachment45,46, and soil protection in the desert areas47, the regions with less than 30% vegetation cover in the study area based on field observation was investigated and showed in Fig. 10. Field observation demonstrated that most areas along with the Jazinak sand corridor and Zabol city have 1–15% and 15–30%36, which are in the priority for stabilization.Figure 10The critical dust hotspot and dust origins in the study area © 2022 by Springer Nature Limited is licensed under Attribution 4.0 International (created by ArcMap 10.5).Full size imageThe results are consistent with Abbasi et al.37, reported that the Hamun Baringak Lake plays a crucial role in the aeolian mobilization of sediments in the Sistan region because of the hydrological droughts that led to the gradual decline of the wetland vegetation cover. Notably, Jahantigh48, in the same study area, reported that the average forage yield of Aeluropus lagopoides in Hamun Hirmand lake in the condition of the water inflow and during drought, was estimated to be 8869 and 173 kg/ha, respectively. It can be explained by the effect of water presence on plant production and cover. However, the average of bare soil of Hamun lake was estimated to be 7.5% and 84.2% in the two periods of water inflow and drought, respectively48. It indicated the impact of dusty days. Therefore, the mentioned areas with the vegetation cover below 30% prioritized for stabilization techniques to dust reduction or mitigation.The detailed field investigation of the land use and vegetation cover, as shown in Fig. 12, indicated the presence of native plants such as A. lagopoides and Tamarix spp. Based on Fig. 11, among the Tamarix genus, the three species of T. aphylla, T. stricta, and T.hispida were observed in the study area. T. stricta is a native species to Iran with benefits including, traditional therapeutic uses in Persian Medicine49,50. Also, the soil EC in the habitat of T. aphylla (15.70 mhos/cm) is almost the same as the control area (15.80 mhos/cm) in the depth of 0–30 cm; while the available potassium in T. aphylla habitat (460 mg/l) was also more than the control area (180 mg/l)51. Hence, the afforestation of Tamarix spp. has caused the addition of soil amendments and increased the clods.Figure 11The most land use/cover in the study area.Full size imageConsequently, the water requirement of the plants in the desert area consisting of T.aphylla, is reported in Table 6. The water requirement of T. stricta was estimated based on Table 6 to be 580 m3/ha for 500 plants no./ha with a vegetation cover of 10–30%.Table 6 Annual water requirement of the T. aphylla for irrigation in the early stages of establishment in terms of planting density (Rad, 2018).Full size tableMoreover, Fig. 12 shows the vast (50% more) soil coverage of T. stricta in the collar area compared to T. aphylla. Therefore, it is more appropriate to cultivate T. stricta than T. aphylla for the biological restoration of the region. Note that the introduced dust mitigation technique using TSE of Zabol WWT can play a specific role in the rehabilitation of soil cover in the mentioned area due to the low water need of native plants. Consequently, it has a significant impact on dust reduction in Zabol city.Figure 12The picture of (a) T. stricta and (b) T. aphylla in the study area.Full size imageHence, based on the hotspots of dust origins in the study area, the most appropriate sites for the project executions of TSE were selected, as shown in Fig. 13. Investigations indicated that a total of 27,500 ha are suitable for the project excision. Hence, considering the water requirement of 500 m3/ha/year, TSE volume of 5.1 mcm/year, vegetation cover of below 30%, and other observations such as the soil coverage in the collar area, the native plant of T. stricta selected for the afforestation of 10,000 ha on the west part of Zabol. This region has the priority in stabilization due to companionship to the corridors with a vegetation cover of 16–30%.Figure 13Area suggested for the dust mitigation project execution by the application of TSE © 2022 by Springer Nature Limited is licensed under Attribution 4.0 International (created by ArcMap 10.5).Full size imageCost analysisFinally, due to the vast area of TSE application, the total of 27,500 ha, with the puprose of dust mitigation, the project execution costs must have been addressed. Hence, Fig. 13 shows the distance of Zabol city to Hamun Hirmand and Baringak lake for transportation calculation. Accordingly, the distance from Zabol to Hamun Hirmand and Baringak lake is 14 and 33 km, respectively. The whole area around Zabol city to Hammon Hirmand lake is cultivated lands; hence, the existing roads reduced construction costs.The two main modes of transportation are trucks and pipelines. There are various pros and cons to both methods. Truck transportation is favored for low volume and short distances, while its costs rapidly increase for large-scale transportation. On the other hand, pipeline transportation is appropriate for large volumes, and long travel distances as it has a positive impact on reducing greenhouse gas emissions. Using pipelines also reduces noise, reduces highway traffic, and improves highway safety.Based on the literature, the variable and fixed transportation cost components depend on the type of product shipped, design requirements, and other decisions related to facility planning. For the sewage sludge with a pH level of 7.0 ± 0.1; hence, a low-cost PVC pipe suggested. Moreover, for cost optimization, as the WWT facilities in the study area do not generate enough volume daily, it makes economical sense to store sewage for a few days to increase the shipped volume. However, reducing the storage to a single day condenses these investment costs drastically52.It was estimated that the total costs for a facility-owned and rented single trailer truck with a capacity of 30 m3 to be $5.6/m3 and 7.4/m3/km, respectively53. Hence, the variable unit transportation cost along a pipeline with a capacity of 480 m3/day is estimated to be $0.144/m3/km. In despite of previous studies mentioning that it is more economical to use a pipeline rather than a rented single trailer truck if the volume shipped is greater than 700 m3/day, in the study area, it is more economical to use a facility-owned single trailer truck, while the shipped volume is 1200 m3/day due to the low cost of petroleum and very close distance of the suggested area. More

von Wintersdorff, C. J. et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front. Microbiol. 7, 173 (2016).
Google Scholar 
Suay-García, B. & Pérez-Gracia, M. T. Present and future of carbapenem-resistant Enterobacteriaceae (CRE) infections. Antibiotics 8, 122 (2019).PubMed Central 
Article 
CAS 

Google Scholar 
Blair, J. M., Webber, M. A., Baylay, A. J., Ogbolu, D. O. & Piddock, L. J. Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 13, 42–51 (2015).CAS 
PubMed 
Article 

Google Scholar 
Codjoe, F. S. & Donkor, E. S. Carbapenem resistance: a review. Med Sci. 6, 1 (2017).
Google Scholar 
Schechner, V. et al. Asymptomatic rectal carriage of blaKPC producing carbapenem-resistant Enterobacteriaceae: who is prone to become clinically infected? Clin. Microbiol. Infect. 19, 451–456 (2013).CAS 
PubMed 
Article 

Google Scholar 
Penders, J., Stobberingh, E. E., Savelkoul, P. H. & Wolffs, P. F. The human microbiome as a reservoir of antimicrobial resistance. Front Microbiol. 4, 87 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Nordmann, P., Naas, T. & Poirel, L. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 17, 1791–1798 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Tooke, C. L. et al. β-Lactamases and β-lactamase inhibitors in the 21st century. J. Mol. Biol. 431, 3472–3500 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sun, X. et al. Microbiota-derived metabolic factors reduce campylobacteriosis in mice. Gastroenterology 154, 1751–1763.e2 (2018).CAS 
PubMed 
Article 

Google Scholar 
Ichinohe, T. et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl Acad. Sci. USA 108, 5354–5359 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Buffie, C. G. et al. Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile. Nature 517, 205–208 (2015).CAS 
PubMed 
Article 

Google Scholar 
Lieberman, T. D. et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat. Genet. 43, 1275–1280 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Garud, N. R., Good, B. H., Hallatschek, O. & Pollard, K. S. Evolutionary dynamics of bacteria in the gut microbiome within and across hosts. PLoS Biol. 17, e3000102 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Chu, N. D., Smith, M. B., Perrotta, A. R., Kassam, Z. & Alm, E. J. Profiling living bacteria informs preparation of fecal microbiota transplantations. PLoS ONE 12, e0170922 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Ferreiro, A., Crook, N., Gasparrini, A. J. & Dantas, G. Multiscale evolutionary dynamics of host-associated microbiomes. Cell 172, 1216–1227 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Mo, Y. et al. Duration of carbapenemase-producing Enterobacteriaceae carriage in hospital patients. Emerg. Infect. Dis. 26, 2182–2185 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Haverkate, M. R. et al. Duration of colonization with Klebsiella pneumoniae carbapenemase-producing bacteria at long-term acute care hospitals in Chicago, Illinois. Open Forum Infect. Dis. 3, ofw178 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Korach-Rechtman, H. et al. Intestinal dysbiosis in carriers of carbapenem-resistant Enterobacteriaceae. mSphere 5, e00173–20 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Yoshida, N. et al. Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis. Circulation 138, 2486–2498 (2018).CAS 
PubMed 
Article 

Google Scholar 
Lenoir, M. et al. Butyrate mediates anti-inflammatory effects of. Gut Microbes 12, 1–16 (2020).PubMed 
Article 
CAS 

Google Scholar 
Riedel, C. U. et al. Anti-inflammatory effects of bifidobacteria by inhibition of LPS-induced NF-κB activation. World J. Gastroenterol. 12, 3729–3735 (2006).PubMed 
PubMed Central 
Article 

Google Scholar 
Zeng, M. Y., Inohara, N. & Nuñez, G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol. 10, 18–26 (2017).CAS 
PubMed 
Article 

Google Scholar 
Winter, S. E. & Bäumler, A. J. A breathtaking feat: to compete with the gut microbiota, Salmonella drives its host to provide a respiratory electron acceptor. Gut Microbes 2, 58–60 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
Rivera-Chávez, F., Lopez, C. A. & Bäumler, A. J. Oxygen as a driver of gut dysbiosis. Free Radic. Biol. Med. 105, 93–101 (2017).PubMed 
Article 
CAS 

Google Scholar 
Chng, K. R. et al. Metagenome-wide association analysis identifies microbial determinants of post-antibiotic ecological recovery in the gut. Nat. Ecol. Evol. 4, 1256–1267 (2020).PubMed 
Article 

Google Scholar 
Tenaillon, O., Skurnik, D., Picard, B. & Denamur, E. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8, 207–217 (2010).CAS 
PubMed 
Article 

Google Scholar 
Stacy, A. et al. Infection trains the host for microbiota-enhanced resistance to pathogens. Cell 184, 615–627.e17 (2021).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Barreto, H. C., Sousa, A. & Gordo, I. The landscape of adaptive evolution of a gut commensal bacteria in aging mice. Curr. Biol. 30, 1102–1109.e5 (2020).CAS 
PubMed 
Article 

Google Scholar 
Ernst, C. M. et al. Adaptive evolution of virulence and persistence in carbapenem-resistant Klebsiella pneumoniae. Nat. Med. 26, 705–711 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Zhao, S. et al. Adaptive evolution within gut microbiomes of healthy people. Cell Host Microbe 25, 656–667.e8 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Warsi, O. M., Andersson, D. I. & Dykhuizen, D. E. Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation. BMC Evol. Biol. 18, 72 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Hickman, R. A., Munck, C. & Sommer, M. O. A. Time-resolved tracking of mutations reveals diverse allele dynamics during Escherichia coli antimicrobial adaptive evolution to single drugs and drug pairs. Front. Microbiol. 8, 893 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Auriol, C., Bestel-Corre, G., Claude, J. B., Soucaille, P. & Meynial-Salles, I. Stress-induced evolution of Escherichia coli points to original concepts in respiratory cofactor selectivity. Proc. Natl Acad. Sci. USA 108, 1278–1283 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Juers, D. H., Matthews, B. W. & Huber, R. E. LacZ β-galactosidase: structure and function of an enzyme of historical and molecular biological importance. Protein Sci. 21, 1792–1807 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Rogers, A. W. L., Tsolis, R. M. & Bäumler, A. J. Salmonella versus the microbiome. Microbiol. Mol. Biol. Rev. 85, e00027–19 (2021).CAS 
PubMed 
Article 

Google Scholar 
Hughes, E. R. et al. Microbial respiration and formate oxidation as metabolic signatures of inflammation-associated dysbiosis. Cell Host Microbe 21, 208–219 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Gupta, S., Allen-Vercoe, E. & Petrof, E. O. Fecal microbiota transplantation: in perspective. Ther. Adv. Gastroenterol. 9, 229–239 (2016).Article 

Google Scholar 
Wortelboer, K., Nieuwdorp, M. & Herrema, H. Fecal microbiota transplantation beyond Clostridioides difficile infections. EBioMedicine 44, 716–729 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Lee, S. M. et al. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426–429 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Martinson, J. N. V. et al. Rethinking gut microbiome residency and the Enterobacteriaceae in healthy human adults. ISME J. 13, 2306–2318 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Woyke, T., Doud, D. F. R. & Schulz, F. The trajectory of microbial single-cell sequencing. Nat. Methods 14, 1045–1054 (2017).CAS 
PubMed 
Article 

Google Scholar 
Domingo, E. & Perales, C. Viral quasispecies. PLoS Genet. 15, e1008271 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Yamada, C. et al. Molecular insight into evolution of symbiosis between breast-fed infants and a member of the human gut microbiome Bifidobacterium longum. Cell Chem. Biol. 24, 515–524.e5 (2017).CAS 
PubMed 
Article 

Google Scholar 
Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Gao, S., Bertrand, D., Chia, B. K. & Nagarajan, N. OPERA-LG: efficient and exact scaffolding of large, repeat-rich eukaryotic genomes with performance guarantees. Genome Biol. 17, 102 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Gao, S., Bertrand, D. & Nagarajan, N. FinIS: improved in silico finishing using an exact quadratic programming formulation. Lect. Notes Comput. Sci. 7534, 314–325 (2012).Article 

Google Scholar 
Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv 1303.3997v2 (2013).Segata, N. et al. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods 9, 811–814 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Franzosa, E. A. et al. Species-level functional profiling of metagenomes and metatranscriptomes. Nat. Methods 15, 962–968 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Salter, S. J. et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12, 87 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
Hawinkel, S., Mattiello, F., Bijnens, L. & Thas, O. A broken promise: microbiome differential abundance methods do not control the false discovery rate. Brief. Bioinformatics 20, 210–221 (2019).PubMed 
Article 

Google Scholar 
Morton, J. T. et al. Establishing microbial composition measurement standards with reference frames. Nat. Commun. 10, 2719 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Inouye, M. et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 6, 90 (2014).PubMed 
PubMed Central 
Article 

Google Scholar 
Alcock, B. P. et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48, D517–D525 (2020).CAS 
PubMed 
Article 

Google Scholar 
Kurtz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).PubMed 
PubMed Central 
Article 

Google Scholar 
Wilm, A. et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res. 40, 11189–11201 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Hinrichs, A. S. et al. The UCSC Genome Browser Database: update 2006. Nucleic Acids Res. 34, D590–D598 (2006).CAS 
PubMed 
Article 

Google Scholar 
Pracana, R., Priyam, A., Levantis, I., Nichols, R. A. & Wurm, Y. The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB. Mol. Ecol. 26, 2864–2879 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Quinlan, A. R. BEDTools: the Swiss-Army tool for genome feature analysis. Curr. Protoc. Bioinformatics 47, 11.12.1–34 (2014).Article 

Google Scholar 
Spedicato, G. Discrete time Markov chains with R. R J. 9.2, 84 (2017).Article 

Google Scholar 
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Hahsler, M., Piekenbrock, M. & Doran, D. dbscan: fast density-based clustering with R. J. Stat. Softw. 91, 1–30 (2019).Article 

Google Scholar 
Galata, V., Fehlmann, T., Backes, C. & Keller, A. PLSDB: a resource of complete bacterial plasmids. Nucleic Acids Res. 47, D195–D202 (2019).CAS 
PubMed 
Article 

Google Scholar 
Ondov, B. D. et al. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 17, 132 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Quan, S. et al. Adaptive evolution of the lactose utilization network in experimentally evolved populations of Escherichia coli. PLoS Genet. 8, e1002444 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Tsuchido, T., VanBogelen, R. A. & Neidhardt, F. C. Heat shock response in Escherichia coli influences cell division. Proc. Natl Acad. Sci. USA 83, 6959–6963 (1986).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Trubetskoy, D., Proux, F., Allemand, F., Dreyfus, M. & Iost, I. SrmB, a DEAD-box helicase involved in Escherichia coli ribosome assembly, is specifically targeted to 23S rRNA in vivo. Nucleic Acids Res. 37, 6540–6549 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Garoff, L., Huseby, D. L., Praski Alzrigat, L. & Hughes, D. Effect of aminoacyl-tRNA synthetase mutations on susceptibility to ciprofloxacin in Escherichia coli. J. Antimicrob. Chemother. 73, 3285–3292 (2018).CAS 
PubMed 
Article 

Google Scholar 
Aponte, R. A., Zimmermann, S. & Reinstein, J. Directed evolution of the DnaK chaperone: mutations in the lid domain result in enhanced chaperone activity. J. Mol. Biol. 399, 154–167 (2010).CAS 
PubMed 
Article 

Google Scholar 
Mundhada, H. et al. Increased production of l-serine in Escherichia coli through adaptive laboratory evolution. Metab. Eng. 39, 141–150 (2017).CAS 
PubMed 
Article 

Google Scholar 
Conrad, T. M. et al. RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl Acad. Sci. USA 107, 20500–20505 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Li, Y. et al. LPS remodeling is an evolved survival strategy for bacteria. Proc. Natl Acad. Sci. USA 109, 8716–8721 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar  More

Spatial–temporal characteristics of land use changeAs shown in Fig. 2, cultivated land was the dominant land use type in Shandong Province during the past 40 years, which accounted for 69.86% (1980), 69.98% (1990), 69.25% (2000), 68.00% (2010) and 66.88% (2020) respectively. Moreover, it was found that the area of cultivated land, forest land, grassland, unused land and ocean gradually decreased, whereas the water area and URL (urban and rural industrial and mining residential land) increased obviously. In particular, grassland decreased by 7542.87 km2 in the past 40 years with a decline rate of 37.18%, which was much higher than cultivated land and forest land. This phenomenon was attributed to the fact that cultivated land and forest land were less susceptible to encroachment as their high vegetation coverage, while grassland was easily occupied by other land types. The serious occupation by other land types has led to a significant reduction in unused land with a very high decline ratio of 64.32% from 2010 to 2020. In contrast to unused land, URL increased significantly at this period (Fig. 3), which was due to the rapidly economic development.Figure 2Land use type map of Shandong Province from 1980 to 2020.Full size imageFigure 3Sankey diagram of land use transfer in different periods.Full size imageThe total area of land use conversion in Shandong Province was 86,909 km2 during the past 40 years, the most drastic change was observed from 2010 to 2020. On the one hand, the major project of new and old kinetic energy conversion in Shandong Province had been implemented since 2000, which led to the expansion of urban land and dramatic changes in land use patterns. On the other hand, social, economic, technological and other factors had a direct impact on land use change by influencing people’s decision-making on land use (e.g., demand for land products, investment in land, protection of land resources, etc.)45,46,47,48. Statistics showed that GDP (Gross Domestic Product) and population density of Shandong Province had increased significantly since 21st century. The GDP of 2010–2020 was about 10 times that of 1980–2000 and population density had also increased by 1.4 times (Data from: Shandong statistical yearbook, http://tjj.shandong.gov.cn/col/col6279/index.html). As the most direct reflection of human activities, land use change was obviously affected by factors such as agricultural cultivation, industrial and mining construction, and urbanization driven by population growth49,50.The most significant changes of land use type were URL (increased by 17.75%), grassland (decreased by 8.72%) and cultivated land (decreased by 7.26%) over the past forty years. URL was mostly converted from cultivated land (26,306 km2) and grassland (1684 km2), which reflected the serious situation of occupying cultivated land in the process of urbanization in Shandong Province. It was caused by tight land use scale and relatively flat terrain of grassland. Besides, the range of land use type in the four periods also exhibited great variations. The conversion of land use from 1980 to 1990 was concentrated in the Yellow River Delta, Laizhou Bay and Weishan Lake, for the same as 1990–2000. At the period of 2000 to 2010, the conversion types concentrated in Bohai Bay and Yellow River Delta. The land use conversion was violent and widely distributed from 2010 to 2020, which was different from previous periods from 1980 to 2010. The conversion of cultivated land → URL and URL → cultivated land were widely distributed in Shandong Province, while another conversion of grassland → cultivated land and forest → cultivated land were concentrated in the Central and South Shandong Mountains and Jiaodong Hills. In addition, the conversion of cultivated land → water area and URL → water area were concentrated in Bohai Bay, Yellow River Delta and Laizhou Bay. Ample water, flat terrain and fertile soils in these bays and deltas facilitates agricultural cultivation and other productive activities. Therefore, the conversion of land use types from 1980 to 2010 was mainly concentrated here (Fig. 4). Specifically, the conversion of water area → URL was 1083 km2 from 1980 to 1990, unused land → water area was 925 km2 from 1990 to 2000, cultivated land → water area was 687 km2 from 2000 to 2010. However, the pattern of land use change dominated by natural factors has been broken in the process of increasing demand for social development and continuous advancement of science and technology. The conversion of land use types has become more dispersed in spatial distribution and the types of conversion have become more diverse.Figure 4Spatial distribution map of land use conversion types in different periods.Full size imageIn fact, one issue of concern in the early exploitation of water was the ecological problems caused by over-exploitation. For example, the cut-off of the Yellow River downstream made it difficult to guarantee the water security of industrial and agricultural production and residential life in the areas along the way. At the same time, the safety of coastal ecosystems was threatened and the phenomenon of soil salinization had become more serious. To alleviate these problems, government and the public have taken a series of measures such as establishing the Yellow River Delta National Nature Reserve was established in 1992, returning farmland to lakes and wetlands, and improving the landscape pattern of rivers and lakes by carrying out ecological treatment in the coastal zone of rivers and lakes51,52. By 2020, the area of water has increased by 50% compared to 1980, while many ecological security issues have been mitigated.Spatial–temporal characteristics of habitat degradationThe spatial–temporal variation of land use types were conducted to explore the variation trend of its habitat quality in Shandong Province. The InVEST-HQ was applied to obtain layers of habitat degradation in different periods. According to the interval range of 0–0.03, 0.03–0.07 and 0.07–0.18, habitat degradation was divided into three levels: slight, moderate and high degradation35,38.As shown in Fig. 5, the habitat quality in Shandong Province was dominated by moderate degradation, with the proportion of 73.30% (1980), 73.25% (1990), 72.49% (2000), 70.45% (2010) and 64.33% (2020), respectively. The spatial pattern of habitat quality was consistent with cultivated land, indicating that cultivated land who was affected by natural and anthropogenic activities exhibited moderate degradation. The proportion of moderate degradation has decreased due to cultivated land have been encroached upon for construction in the process of development, thus habitat degradation has become more and more serious. Although some of the moderate degraded areas were also converted to slight degraded areas, the area of conversion was very small compared to its conversion to high degraded areas.Figure 5Distribution map of habitat degradation in Shandong Province from 1980 to 2020.Full size imageThe proportion of slight degradation ranges from 22.38% to 24.89%, it was concentrated in the Yellow River Delta, the Central and South of Shandong Mountains, Weishan Lake and Jiaodong Hills, which was less disturbed by human activities. Compared with 1980, the proportion of slight degraded areas increased marginally in 2020, and its change was a fluctuating process. The proportion of slight degraded areas decreased from 1980 to 1990, and its proportion slowly increased from 1990 to 2020. This dynamic change process could be verified according to the spatial distribution characteristics in the Yellow River Delta. The habitat quality of the Yellow River Delta, which originally showed slight degradation, showed high degradation in 1990, 2000 and 2010.The proportion of high degradation ranges from 4.03% to 10.78%, which was concentrated in the built-up area of the city where human activities were more intensive. The proportion of high degraded areas has been increasing, indicating that the habitat has been degraded severely and its quality has declined. As the proportion of high degraded areas raised, two patterns of their spatial distribution also emerged. First spatial pattern was concentrated in urban built-up areas because of the high degree of human exploitation of land, which led to significant habitat degradation. The second pattern was a circle structure with “slight degradation” as the center and “high degradation-moderate degradation-slight degradation” outward, which was similar to the spatial distribution structure of habitat degradation in Fujian Province studied by Li et al.40. The circle structure was formed in 2010, and the distribution range was significantly expanded in 2020. The reason for the formation was that the built-up land in the city center has been severely damaged, and the possibility of re-degradation was reduced, instead showing “slight degradation”. However, the adjacent urban areas were more threatened and severely degraded, presenting “high degradation”. With the increase of distance, habitat threat and degradation decreased gradually, displaying “slight degradation”.Spatial–temporal evolution characteristics of habitat qualityThe InVEST-HQ was used to obtain layers of habitat quality in different periods. As summarized in Table 4, habitat quality was divided into five levels by the interval range: low (0–0.2), relatively low (0.2–0.4), medium (0.4–0.6), relative high (0.6–0.8), and high (0.8–1.0)35,38.Table 4 The proportion of habitat quality level at different periods in Shandong Province.Full size tableOur study concluded that the level of habitat quality in Shandong Province declined from 1980 to 2020.The results showed an overall decline of 4.75% in Shandong Province. Among them, the most significant rate of decline was observed in 2010–2020 (1.86%), which was similar to the phase change characteristics of land use types. At this period, the “Development Plan of Yellow River Delta Efficient Ecological Economic Zone” and the “Development Plan of Shandong Peninsula Blue Economic Zone” have become national development strategies. The demonstration area of “Bohai granary” and the restructuring of steel industry were carried out simultaneously. Meanwhile, the Beijing-Shanghai high-speed railway (Shandong section), Qingdao Jiaozhou Bay Bridge, Jiaozhou Bay Tunnel have strengthened the connection between Shandong Province and the outside world. As a result, rapid development has led to a rapid decline in the quality of its habitat. The rate of decline in 1980–1990 (1.43%) and 2000–2010 (1.42%) was comparable and the rate of decline in 1990–2000 was the lowest at 0.12%, which was significantly related to the development level of cities in each period. The period of 1980–1990 and 2000–2010 were in the initial and rapid promotion stages of reform and opening-up respectively. The initial stage was led by rural reform, and urban reform was launched on a pilot basis. The rapid advancement stage was led by urban reform, and economic development entered a healthy track of steady progress. Therefore, the proportion of habitat quality changes in the two periods was comparable. The period of 1990–2000 was in the exploration and transition stage of reform and opening-up, whose development process was relatively stable, resulting in the lowest rate of change in habitat quality.The average value of habitat quality in Shandong Province was 1980 (0.5091), 1990 (0.5018), 2000 (0.5012), 2010 (0.4941) and 2020 (0.4849), which decreased during the entire period. Habitat quality was dominated by medium-level throughout the whole period, with the proportion in 1980 (68.95%), 1990 (68.54%), 2000 (67.74%), 2010 (66.37%) and 2020 (65.47%). The land type in this category was mainly cultivated land (Fig. 6), which was continuous encroachment during the study period, resulting in a decrease in the percentage of medium-level habitat quality. From 1980 to 2020, the percentage of low-level habitat quality increased from 12.67% to 17.44%, and the relatively low-level decreased from 0.46% to 0.23%. The main reason was the continuous increasing of construction land and the degree of habitat threat led to the decreasing of habitat suitability. Therefore, the area of low-level habitat quality showed an increasing trend. Low and relative low-level habitat quality areas were concentrated in the urban areas of coastal and inland cities, and the Yellow River Delta. Urban areas, with a large scale of industry, commerce and population, also have a high level of urbanization. The original natural habitat has been modified during the development process, which resulted low-level habitat quality. The habitat quality of the Yellow River Delta was dynamic. The low-level pattern formed by early over-exploitation was improved in later conservation and development. The proportion of high-level habitat quality increased from 11.64% to 12.98%, and the relatively high-level decreased from 6.28% to 3.88%. In terms of spatial distribution, it was concentrated in the Central and South Shandong Mountains, Jiaodong Hills, the Yellow River Delta (2020), Weishan Lake and Wulian Mountain. These areas were dominated by mountains and well-protected water, which had high habitat suitability and were less stressed by surrounding construction land, thus maintaining high-level habitat quality. The increase of high-level habitat quality was due to the influence of water with high habitat suitability, which expanded a lot in the past 40 years, leading to the spread of high-level regional habitat quality, especially in the Yellow River Delta.Figure 6Distribution map of habitat quality in Shandong Province from 1980 to 2020.Full size imageThe value of Moran’s I was 0.3935 (1980), 0.3852 (1990), 0.4031 (2000), 0.4186 (2010) and 0.4644 (2020), respectively, which revealed that the spatial agglomeration of habitat quality in Shandong Province was characterized by agglomeration, and the trend of agglomeration increased obviously after 2000.As shown in Fig. 7, the habitat quality in Shandong Province exhibited obvious spatial heterogeneity, and spatial distribution of cold and hot spot was consistent with the topographic features. Hot spot (high-value area of habitat quality) presented “two primary and two secondary + Yellow River Delta”. Two primary hot spots distributed in the Central and South Shandong Mountains and the Jiaodong Hills, the two secondary hot spots located in Weishan Lake and Wulian Mountain. The formation of above hot spot was mainly due to high altitudes or steep slopes conferred favorable habitat quality, which was associated with the accessibility of human activities. Human accessibility at high altitudes or steep slopes was limited, so it was unlikely to cause major interference with the original environment53,54. However, the formation of other hot spot in Yellow River Delta was due to protective human activities. Cold spot (low-value area of habitat quality) was scattered in the northwestern Plain of Shandong Province, provincial capital metropolitan area and peninsula urban agglomeration which was dominated by cultivated land and built-up land in the cities that was affected by agricultural cultivation and industrial activities.Figure 7Distribution map of hot and cold spots of habitat quality in Shandong Province from 1980 to 2020.Full size imageOverall, the spatial distribution pattern of habitat quality in Shandong Province was relatively stable and affected by many factors, among which land use change was the most important one9,40,55. The most dominant land type in Shandong Province was cultivated land, which was concentrated in the northwest plain. Influenced by agricultural farming, the habitat quality of cultivated land presented medium-level category. At the same time, the habitat quality of some cultivated land has decreased due to the influence of construction land intrusion. The high vegetation coverage and rich species diversity of mountains and hills make their natural habitat quality superior. With the development of urban economy, the scale of construction land in coastal lowlands as well as inland urban areas continued to expand. The increase in population density as well as the intensity of land use activities has led to the expansion of regional dehabitatization. In addition, the dynamic changes in the habitat quality of the Yellow River Delta indicated that differences in the degree of land use change led to a variety of impacts on habitat quality. Therefore, habitat quality improvement and ecological protection should be based on local regional resource endowments and follow the concept of comprehensive, coordinated and sustainable development. Administration should formulate differentiated ecological protection strategies. For urban land development, authorities should increase the intensive utilization of construction land, limit the development boundaries of urban land and increase the greening rate inside urban land, such as equipped with urban green space park and other ecological land. In order to ensure the efficiency of agricultural production in Shandong Province, authorities should pay special attention to the conservation of cultivated land and to the development of ecological agriculture56. For natural ecosystems such as forest and grassland, authorities should improve the natural reserve system57. The vegetation ecological restoration project should be carried out according to local conditions. Drawing on the effective experience of ecological changes in the Yellow River Delta, we would take it as a typical example in future development and adopt corresponding administrative methods to coordinate the relationship between economy and habitat quality and change the dilemma of low-level habitat quality areas. Therefore, it is necessary to implement reasonable and effective territorial space planning to achieve regional sustainable development. More

Hawkes, C. V., Bull, J. J. & Lau, J. A. Symbiosis and stress: how plant microbiomes affect host evolution. Philos. T. R. Soc. B. 375, 20190590 (2020).CAS 
Article 

Google Scholar 
Leopold, D. R. & Busby, P. E. Host Genotype and Colonist Arrival Order Jointly Govern Plant Microbiome Composition and Function. Curr. Biol. 30, 3260–3266 (2020).CAS 
PubMed 
Article 

Google Scholar 
Morella, N. M. et al. Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. Proc. Natl Acad. Sci. USA 117, 1148–1159 (2020).CAS 
PubMed 
Article 

Google Scholar 
Garcia, J. & Kao-Kniffin, J. Microbial Group Dynamics in Plant Rhizospheres and Their Implications on Nutrient Cycling. Front. Plant Sci. 9, 1516 (2018).Article 

Google Scholar 
Marschner P. Plant-Microbe Interactions in the Rhizosphere and Nutrient Cycling in Nutrient Cycling in Terrestrial Ecosystems (eds. Marschner, P. & Rengel, Z.) 159–183 (Springer, 2007).Vannier, N., Agler, M. & Hacquard, S. Microbiota-mediated disease resistance in plants. PLoS Pathog. 15, e1007740 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Wei, Z. et al. Initial soil microbiome composition and functioning predetermine future plant health. Sci. Adv. 5, 6584 (2019).
Google Scholar 
Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability. Trends Ecol. Evol. 31, 440–452 (2016).PubMed 
Article 

Google Scholar 
Dessaux, Y., Grandclemént, C. & Faure, D. Engineering the Rhizosphere. Trends Plant Sci. 21, 266–278 (2016).CAS 
PubMed 
Article 

Google Scholar 
Swenson, W., Wilson, D. S. & Elias, R. Artificial ecosystem selection. Proc. Natl Acad. Sci. USA 97, 9110–9114 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Panke-Buisse, K., Poole, A., Goodrich, J., Ley, R. E. & Kao-Kniffin, J. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 9, 980–989 (2015).CAS 
PubMed 
Article 

Google Scholar 
van den Bergh, B. et al. Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution. Microbiol. Mol. Biol. Rev. 82, e00008–e00018 (2018).PubMed 
PubMed Central 

Google Scholar 
Garcia, J. & Kao-Kniffin, J. Can dynamic network modelling be used to identify adaptive microbiomes? Funct. Ecol. 34, 2065–2074 (2020).Article 

Google Scholar 
Faust, K. & Raes, J. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538–550 (2012).CAS 
PubMed 
Article 

Google Scholar 
Wilson, D. & Wilson, E. Evolution “for the good of the group”. Am. Sci. 96, 380–389 (2008).Article 

Google Scholar 
de la Fuente Cantó, C. et al. An extended root phenotype: the rhizosphere, its formation and impacts on plant fitness. Plant J. 103, 951–964 (2020).PubMed 
Article 
CAS 

Google Scholar 
Sachs, J., Mueller, U., Wilcox, T. & Bull, J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).PubMed 
Article 

Google Scholar 
Harrington, K. & Sanchez, A. Eco-evolutionary dynamics of complex social strategies in microbial communities. Commun. Integr. Biol. 7, e28230 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Rauch, J., Kondev, J. & Sanchez, A. Cooperators trade off ecological resilience and evolutionary stability in public goods games. J. R. Soc. Interface 14, 20160967 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Sexton, D. & Schuster, M. Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation. Nat. Commun. 8, 230 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Schmidt, J. E., Kent, A. D., Brisson, V. L. & Gaudin, A. C. M. Agricultural management and plant selection interactively affect rhizosphere microbial community structure and nitrogen cycling. Microbiome 7, 146 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Turner, T. et al. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere. microbiome plants ISME J. 7, 2248–2258 (2013).CAS 
PubMed 

Google Scholar 
Jones, D. L., Nguyen, C. & Finlay, R. D. Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321, 5–33 (2009).CAS 
Article 

Google Scholar 
George, E., Marschner, H. & Jakobsen, I. Role of Arbuscular Mycorrhizal Fungi in Uptake of Phosphorus and Nitrogen From Soil. Crit. Rev. Biotechnol. 15, 257–270 (1995).Article 

Google Scholar 
Hodge, A. & Fitter Alastair, H. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl Acad. Sci. USA 107, 13754–13759 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Lambers, H. & Teste, F. P. Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do non-mycorrhizal species at both extremes of nutrient availability play the same game. Plant Cell Environ. 36, 1911–1915 (2013).PubMed 

Google Scholar 
Delaux, P. M. et al. Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet. 10, e1004487 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Anas, M. et al. Fate of nitrogen in agriculture and environment: agronomic, eco-physiological and molecular approaches to improve nitrogen use efficiency. Biol. Res. 53, 47 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Madhaiyan, M. et al. Arachidicoccus rhizosphaerae gen. nov., sp. nov., a plant-growth-promoting bacterium in the family Chitinophagaceae isolated from rhizosphere soil. Int. J. Syst. Evol. Microbiol. 65, 578–586 (2015).CAS 
PubMed 
Article 

Google Scholar 
Song, H. et al. Environmental filtering of bacterial functional diversity along an aridity gradient. Sci. Rep. 9, 866 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Xia, L. C. et al. Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates. BMC Syst. Biol. 5, S15 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
Kuntal, B. K., Chandrakar, P., Sadhu, S. & Mandhi, S. S. ‘NetShift’: a methodology for understanding ‘driver microbes’ from healthy and disease microbiome datasets. ISME J. 13, 442–454 (2019).PubMed 
Article 

Google Scholar 
Layeghifard, M., Hwang, D. M. & Guttman, D. S. Disentangling Interactions in the Microbiome: A Network Perspective. Trends Microbiol. 25, 217–228 (2017).CAS 
PubMed 
Article 

Google Scholar 
Hu, Q. et al. Network analysis infers the wilt pathogen invasion associated with non-detrimental bacteria. NPJ Biofilms Microbiomes 6, 8 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Faust, K. et al. Cross-biome comparison of microbial association networks. Front. Microbiol. 6, 1200 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
Rengel, Z. & Marschner, P. Nutrient availability and management in the rhizosphere: exploiting genotypic differences. N. Phytol. 168, 305–312 (2005).CAS 
Article 

Google Scholar 
Marschner, P. The Role of Rhizosphere Microorganisms in Relation to P Uptake by Plants in The Ecophysiology of Plant-Phosphorus Interactions (eds. White, P. & Hammond, J.) 165–167 (Springer, 2008).Repert, D., Underwood, J., Smith, R. & Song, B. Nitrogen cycling processes and microbial community composition in bed sediments in the Yukon River at Pilot Station. J. Geophys. Res. Biogeosci. 119, 2328–2344 (2014).CAS 
Article 

Google Scholar 
Rolletschek, H. et al. Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol. 137, 1236–1249 (2005).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sanders, A. et al. AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 59, 540–552 (2009).CAS 
PubMed 
Article 

Google Scholar 
Carter, A. M. & Tegeder, M. Increasing nitrogen fixation and seed development in soybean requires complex adjustments of nodule nitrogen metabolism and partitioning processes. Curr. Biol. 26, 2044–2051 (2016).CAS 
PubMed 
Article 

Google Scholar 
Meier, I. C. et al. Root exudation of mature beech forests across a nutrient availability gradient: the role of root morphology and fungal activity. N. Phytol. 226, 583–594 (2020).CAS 
Article 

Google Scholar 
Xu, Y., He, J., Cheng, W., Xing, X. & Li, L. Natural 15N abundance in soils and plants in relation to N cycling in a rangeland in Inner Mongolia. J. Plant Ecol. 3, 201–207 (2010).Article 

Google Scholar 
Henneron, L. et al. Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. N. Phytol. 228, 1269–1282 (2020).CAS 
Article 

Google Scholar 
Hobbie, E. A. & Högberg, P. Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. N. Phytol. 196, 367–382 (2012).CAS 
Article 

Google Scholar 
Zhou, S. et al. Assessing nitrification and denitrification in a paddy soil with different water dynamics and applied liquid cattle waste using the 15N isotopic technique. Sci. Total Environ. 430, 93–100 (2012).CAS 
PubMed 
Article 

Google Scholar 
Fuertes-Mendizábal, T. et al. 15N Natural Abundance Evidences a Better Use of N Sources by Late Nitrogen Application in Bread Wheat. Front. Plant Sci. 9, 853 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Yoneyama, T., Omata, T., Nakata, S. & Yazaki, J. Fractionation of Nitrogen Isotopes during the Uptake and Assimilation of Ammonia by Plants. Plant Cell Physiol. 32, 1211–1217 (1991).CAS 

Google Scholar 
Vacheron, J. et al. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 4, 356 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Granada, C., Passaglia, L., de Souza, E. & Sperotto, R. Is Phosphate Solubilization the Forgotten Child of Plant Growth-Promoting Rhizobacteria? Front. Microbiol. 9, 2054 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Compant, S., Duffy, B., Nowak, J., Clément, C. & Barka, E. Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles, Mechanisms of Action, and Future Prospects. Appl. Environ. Microbiol. 71, 4951 (2005).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Berges, J.A., & Mulholland, M.R. Enzymes and nitrogen cycling in Nitrogen in the marine environment (eds. Capone, D., Bronk, D., Mulholland, M., & Carpenter, E.) 1385–1444 (Elsevier 2008).DeAngelis, K. M., Lindow, S. E. & Firestone, M. Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microb. Ecol. 66, 197–207 (2008).CAS 
Article 

Google Scholar 
Evans, S., Martiny, J. & Allison, S. Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J. 11, 176–185 (2017).PubMed 
Article 

Google Scholar 
Ron, R., Fragman-Sapir, O. & Kadmon, R. (2018). Dispersal increases ecological selection by increasing effective community size. Proc. Natl Acad. Sci. USA. 115, 11280–11285 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Busby, P. et al. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol. 15, e2001793 (2017).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Sergaki, C., Lagunas, B., Lidbury, I., Gifford, M. & Schäfer, P. Challenges and Approaches in Microbiome Research: From Fundamental to Applied. Front. Plant Sci. 9, 1205 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Herlemann, D. P. et al. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5, 1571–1579 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Garcia, J. et al. Selection pressure on the rhizosphere microbiome alters nitrogen use efficiency and seed yield in Brassica rapa. National Center for Biotechnology Information Repository. https://www.ncbi.nlm.nih.gov/sra/PRJNA833111 (2022).Ruan, Q. et al. Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics 22, 2532–2538 (2006).CAS 
PubMed 
Article 

Google Scholar 
Pollet, T. et al. Prokaryotic community successions and interactions in marine biofilms: the key role of Flavobacteria. FEMS Microbiol. Ecol. 94, fiy083 (2018).
Google Scholar 
Durno, W. E. et al. Expanding the boundaries of local similarity analysis. BMC Genomics 14, S3 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Garcia, J. et al. Selection pressure on the rhizosphere microbiome alters nitrogen use efficiency and seed yield in Brassica rapa. https://doi.org/10.5281/zenodo.6800595 (2022). More

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

Google Scholar 
Inagaki, F. et al. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349, 420–424 (2015).CAS 
PubMed 
Article 

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

Google Scholar 
D’Hondt, K. et al. Microbiome innovations for a sustainable future. Nat. Microbiol. 6, 138–142 (2021).PubMed 
Article 
CAS 

Google Scholar 
Lloyd, K. G., Steen, A. D., Ladau, J., Yin, J. & Crosby, L. Phylogenetically novel uncultured microbial cells dominate earth microbiomes. mSystems 3, e00055-18 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Lewis, W. H., Tahon, G., Geesink, P., Sousa, D. Z. & Ettema, T. J. G. Innovations to culturing the uncultured microbial majority. Nat. Rev. Microbiol. 19, 225–240 (2021).CAS 
PubMed 
Article 

Google Scholar 
Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2021).CAS 
PubMed 
Article 

Google Scholar 
Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).CAS 
PubMed 
Article 

Google Scholar 
Hugenholtz, P. Exploring prokaryotic diversity in the genomic era. Genome Biol. 3, REVIEWS0003 (2002).PubMed 
PubMed Central 
Article 

Google Scholar 
Engelen, B. & Imachi, H. Cultivation of subseafloor prokaryotic life in developments in marine geology. In Earth and Life Processes Discovered from Subseafloor Environment. Vol. 7 (eds. Stein, R., Blackman, D., Inagaki, F. & Larsen, H.-L.) 197–209 (Elsevier, 2014).Baker, B. J., Appler, K. E. & Gong, X. New microbial biodiversity in marine sediments. Annu. Rev. Mar. Sci. 13, 161–175 (2021).Article 

Google Scholar 
Hoshino, T. et al. Global diversity of microbial communities in marine sediment. Proc. Natl Acad. Sci. USA 117, 27587–27597 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Tahon, G., Geesink, P. & Ettema, T. J. G. Expanding archaeal diversity and phylogeny: past, present, and future. Annu. Rev. Microbiol. 75, 359–381 (2021).PubMed 
Article 
CAS 

Google Scholar 
Bhattarai, S., Cassarini, C. & Lens, P. N. L. Physiology and distribution of archaeal methanotrophs that couple anaerobic oxidation of methane with sulfate reduction. Microbiol. Mol. Biol. Rev. 83, e00074-18 (2019).PubMed 
PubMed Central 
Article 

Google Scholar 
Krukenberg, V. et al. Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia. Environ. Microbiol. 20, 1651–1666 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Wegener, G., Krukenberg, V., Ruff, S. E., Kellermann, M. Y. & Knittel, K. Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane. Front. Microbiol. 7, 46 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
Agrawal, L. K. et al. Treatment of raw sewage in a temperate climate using a UASB reactor and the hanging sponge cubes process. Water Sci. Technol. 36, 433–440 (1997).CAS 
Article 

Google Scholar 
Tyagi, V. K. et al. Future perspectives of energy saving down-flow hanging sponge (DHS) technology for wastewater valorization—a review. Rev. Environ. Sci. Biotechnol. 20, 389–418 (2021).Article 

Google Scholar 
Namita Maharjan, N. et al. Downflow hanging sponge system: a self-sustaining option for wastewater treatment. In Wastewater Treatment (IntechOpen, London, UK, 2020) Available at https://www.intechopen.com/online-first/74120Nurmiyanto, A. & Ohashi, A. Downflow hanging sponge (DHS) reactor for wastewater treatment—a short review. MATEC Web Conf. 280, 05004 (2019).CAS 
Article 

Google Scholar 
Hatamoto, M., Okubo, T., Kubota, K. & Yamaguchi, T. Characterization of downflow hanging sponge reactors with regard to structure, process function, and microbial community compositions. Appl. Microbiol. Biotechnol. 102, 10345–10352 (2018).CAS 
PubMed 
Article 

Google Scholar 
Tandukar, M., Uemura, S., Ohashi, A. & Harada, H. Combining UASB and the ‘fourth generation’ down-flow hanging sponge reactor for municipal wastewater treatment. Water Sci. Technol. 53, 209–218 (2006).CAS 
PubMed 
Article 

Google Scholar 
Chuang, H.-P. et al. Microbial community that catalyzes partial nitrification at low oxygen atmosphere as revealed by 16S rRNA and amoA genes. J. Biosci. Bioeng. 104, 525–528 (2007).CAS 
PubMed 
Article 

Google Scholar 
Imachi, H. et al. Cultivation of methanogenic community from subseafloor sediments using a continuous-flow bioreactor. ISME J. 5, 1913–1925 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Aoki, M. et al. A long-term cultivation of an anaerobic methane-oxidizing microbial community from deep-sea methane-seep sediment using a continuous-flow bioreactor. PLoS ONE 9, e105356 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Kato, S. et al. Biotic manganese oxidation coupled with methane oxidation using a continuous-flow bioreactor system under marine conditions. Water Sci. Technol. 76, 1781–1795 (2017).CAS 
PubMed 
Article 

Google Scholar 
Imachi, H. et al. Cultivable microbial community in 2-km-deep, 20-million-year-old subseafloor coalbeds through ~1000 days anaerobic bioreactor cultivation. Sci. Rep. 9, 2305 (2019).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Imachi, H. et al. Pelolinea submarina gen. nov., sp. nov., an anaerobic, filamentous bacterium of the phylum Chloroflexi isolated from subseafloor sediment. Int. J. Syst. Evol. Microbiol. 64, 812–818 (2014).CAS 
PubMed 
Article 

Google Scholar 
Imachi, H. et al. Sedimentibacter acidaminivorans sp. nov., an anaerobic, amino-acid-utilizing bacterium isolated from marine subsurface sediment. Int. J. Syst. Evol. Microbiol. 66, 1293–1300 (2016).CAS 
PubMed 
Article 

Google Scholar 
Imachi, H. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 577, 519–525 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Miyazaki, M. et al. Sphaerochaeta multiformis sp. nov., an anaerobic, psychrophilic bacterium isolated from subseafloor sediment, and emended description of the genus Sphaerochaeta. Int. J. Syst. Evol. Microbiol. 64, 4147–4154 (2014).PubMed 
Article 
CAS 

Google Scholar 
Miyazaki, M. et al. Spirochaeta psychrophila sp. nov., a psychrophilic spirochaete isolated from subseafloor sediment, and emended description of the genus Spirochaeta. Int. J. Syst. Evol. Microbiol. 64, 2798–2804 (2014).CAS 
PubMed 
Article 

Google Scholar 
Nakahara, N. et al. Aggregatilinea lenta gen. nov., sp. nov., a slow-growing, facultatively anaerobic bacterium isolated from subseafloor sediment, and proposal of the new order Aggregatilineales ord. nov. within the class Anaerolineae of the phylum Chloroflexi. Int. J. Syst. Evol. Microbiol. 69, 1185–1194 (2019).CAS 
PubMed 
Article 

Google Scholar 
Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).CAS 
PubMed 
Article 

Google Scholar 
Liu, Y. et al. Expanded diversity of Asgard archaea and their relationships with eukaryotes. Nature 593, 553–557 (2021).CAS 
PubMed 
Article 

Google Scholar 
Ruff, S. E. et al. Global dispersion and local diversification of the methane seep microbiome. Proc. Natl Acad. Sci. USA 112, 4015–4020 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Chadwick, G. et al. Comparative genomics reveals electron transfer and syntrophic mechanisms differentiating methanotrophic and methanogenic archaea. PLoS Biol. 20, e3001508 (2022).PubMed 
PubMed Central 
Article 

Google Scholar 
Cario, A., Oliver, G. C. & Rogers, K. L. Exploring the deep marine biosphere: challenges, innovations, and opportunities. Front. Earth Sci. 7, 225 (2019).Article 

Google Scholar 
Jørgensen, B. B. & Boetius, A. Feast and famine—microbial life in the deep-sea bed. Nat. Rev. Microbiol. 5, 770–781 (2007).PubMed 
Article 
CAS 

Google Scholar 
Hoehler, T. M. & Jørgensen, B. B. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11, 83–94 (2013).CAS 
PubMed 
Article 

Google Scholar 
Schink, B. & Stams, A. J. M. Syntrophism among prokaryotes. In The Prokaryotes: Prokaryotic Communities and Ecophysiology (eds. Rosenberg, E. et al.) 471–493 (Springer, 2013).de Bok, F. A. M. et al. The first true obligately syntrophic propionate-oxidizing bacterium, Pelotomaculum schinkii sp. nov., co-cultured with Methanospirillum hungatei, and emended description of the genus Pelotomaculum. Int. J. Syst. Evol. Microbiol. 55, 1697–1703 (2005).PubMed 
Article 
CAS 

Google Scholar 
Imachi, H. et al. Pelotomaculum propionicicum sp. nov., an anaerobic, mesophilic, obligately syntrophic, propionate-oxidizing bacterium. Int. J. Syst. Evol. Microbiol. 57, 1487–1492 (2007).PubMed 
Article 

Google Scholar 
Qiu, Y.-L. et al. Syntrophorhabdus aromaticivorans gen. nov., sp. nov., the first cultured anaerobe capable of degrading phenol to acetate in obligate syntrophic associations with a hydrogenotrophic methanogen. Appl. Environ. Microbiol. 74, 2051–2058 (2008).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Matsushita, S. et al. Anti-bacterial effects of MnO2 on the enrichment of manganese-oxidizing bacteria in downflow hanging sponge reactors. Microbes Environ. 35, ME20052 (2020).PubMed Central 

Google Scholar 
Momper, L. et al. Rectinema subterraneum sp. nov, a chemotrophic spirochaete isolated from the deep terrestrial subsurface. Int. J. Syst. Evol. Microbiol. 70, 4739–4747 (2020).CAS 
PubMed 
Article 

Google Scholar 
Chuang, H.-P., Ohashi, A., Imachi, H., Tandukar, M. & Harada, H. Effective partial nitrification to nitrite by down-flow hanging sponge reactor under limited oxygen condition. Water Res. 41, 295–302 (2007).CAS 
PubMed 
Article 

Google Scholar 
Hatamoto, M., Koshiyama, Y., Kindaichi, T., Ozaki, N. & Ohashi, A. Enrichment and identification of methane-oxidizing bacteria by using down-flow hanging sponge bioreactors under low methane concentration. Ann. Microbiol. 61, 683–687 (2010).Article 
CAS 

Google Scholar 
Hatamoto, M., Yamamoto, H., Kindaichi, T., Ozaki, N. & Ohashi, A. Biological oxidation of dissolved methane in effluents from anaerobic reactors using a down-flow hanging sponge reactor. Water Res. 44, 1409–1418 (2010).CAS 
PubMed 
Article 

Google Scholar 
Hatamoto, M., Miyauchi, T., Kindaichi, T., Ozaki, N. & Ohashi, A. Dissolved methane oxidation and competition for oxygen in down-flow hanging sponge reactor for post-treatment of anaerobic wastewater treatment. Bioresour. Technol. 102, 10299–10304 (2011).CAS 
PubMed 
Article 

Google Scholar 
Hatamoto, M. et al. Potential of nitrous oxide conversion in batch and down-flow hanging sponge bioreactor systems. Sustain. Environ. Res. 24, 117–128 (2014).
Google Scholar 
Cao, L. T. T. et al. Biological oxidation of Mn(II) coupled with nitrification for removal and recovery of minor metals by downflow hanging sponge reactor. Water Res. 68, 545–553 (2015).CAS 
PubMed 
Article 

Google Scholar 
Yamaguchi, T. et al. A novel approach for toluene gas treatment using a downflow hanging sponge reactor. Appl. Microbiol. Biotechnol. 102, 5625–5634 (2018).CAS 
PubMed 
Article 

Google Scholar 
Matsushita, S. et al. Production of biogenic manganese oxides coupled with methane oxidation in a bioreactor for removing metals from wastewater. Water Res. 130, 224–233 (2018).CAS 
PubMed 
Article 

Google Scholar 
Onodera, T. et al. Characterization of the retained sludge in a down-flow hanging sponge (DHS) reactor with emphasis on its low excess sludge production. Bioresour. Technol. 136, 169–175 (2013).CAS 
PubMed 
Article 

Google Scholar 
Miyaoka, Y., Hatamoto, M., Yamaguchi, T. & Syutsubo, K. Eukaryotic community shift in response to organic loading rate of an aerobic trickling filter (down-flow hanging sponge reactor) treating domestic sewage. Microb. Ecol. 73, 801–814 (2016).PubMed 
Article 
CAS 

Google Scholar 
Park, M.-O., Ikenaga, H. & Watanabe, K. Phage diversity in a methanogenic digester. Microb. Ecol. 53, 98–103 (2006).PubMed 
Article 
CAS 

Google Scholar 
Wu, Q. & Liu, W.-T. Determination of virus abundance, diversity and distribution in a municipal wastewater treatment plant. Water Res. 43, 1101–1109 (2009).CAS 
PubMed 
Article 

Google Scholar 
Chien, I.-C., Meschke, J. S., Gough, H. L. & Ferguson, J. F. Characterization of persistent virus-like particles in two acetate-fed methanogenic reactors. PLoS One 8, e81040 (2013).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Girguis, P. R., Orphan, V. J., Hallam, S. J. & DeLong, E. F. Growth and methane oxidation rates of anaerobic methanotrophic archaea in a continuous-flow bioreactor. Appl. Environ. Microbiol. 69, 5472–5482 (2003).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Zhang, Y., Maignien, L., Zhao, X., Wang, F. & Boon, N. Enrichment of a microbial community performing anaerobic oxidation of methane in a continuous high-pressure bioreactor. BMC Microbiol. 11, 137 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Sauer, P., Glombitza, C. & Kallmeyer, J. A system for incubations at high gas partial pressure. Front. Microbiol. 3, 25 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
Bhattarai, S. et al. Enrichment of sulfate reducing anaerobic methane oxidizing community dominated by ANME-1 from Ginsburg Mud Volcano (Gulf of Cadiz) sediment in a biotrickling filter. Bioresour. Technol. 259, 433–441 (2018).CAS 
PubMed 
Article 

Google Scholar 
Cassarini, C. et al. Enrichment of anaerobic methanotrophs in biotrickling filters using different sulfur compounds as electron acceptor. Environ. Eng. Sci. 36, 431–443 (2018).Article 
CAS 

Google Scholar 
Cassarini, C. et al. Anaerobic methane oxidation coupled to sulfate reduction in a biotrickling filter: reactor performance and microbial community analysis. Chemosphere 236, 124290 (2019).CAS 
PubMed 
Article 

Google Scholar 
Adams, M. M., Hoarfrost, A. L., Bose, A., Joye, S. B. & Girguis, P. R. Anaerobic oxidation of short-chain alkanes in hydrothermal sediments: potential influences on sulfur cycling and microbial diversity. Front. Microbiol. 4, 110 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Machdar, I., Sekiguchi, Y., Sumino, H., Ohashi, A. & Harada, H. Combination of a UASB reactor and a curtain type DHS (downflow hanging sponge) reactor as a cost-effective sewage treatment system for developing countries. Water Sci. Technol. 42, 83–88 (2000).CAS 
Article 

Google Scholar 
Judd, S. The status of membrane bioreactor technology. Trends Biotechnol. 26, 109–116 (2008).CAS 
PubMed 
Article 

Google Scholar 
Smith, A. L. et al. Perspectives on anaerobic membrane bioreactor treatment of domestic wastewater: a critical review. Bioresour. Technol. 122, 149–159 (2012).CAS 
PubMed 
Article 

Google Scholar 
Meulepas, R. J. W. et al. Enrichment of anaerobic methanotrophs in sulfate-reducing membrane bioreactors. Biotechnol. Bioeng. 104, 458–470 (2009).CAS 
PubMed 
Article 

Google Scholar 
Jagersma, G. C. et al. Microbial diversity and community structure of a highly active anaerobic methane-oxidizing sulfate-reducing enrichment. Environ. Microbiol. 11, 3223–3232 (2009).CAS 
PubMed 
Article 

Google Scholar 
Lettinga, G., van Velsen, A. F. M., Hobma, S. W., de Zeeuw, W. & Klapwijk, A. Use of the upflow sludge blanket (USB) reactor concept for biological wastewater treatment, especially for anaerobic treatment. Biotechnol. Bioeng. 22, 699–734 (1980).CAS 
Article 

Google Scholar 
Sekiguchi, Y., Kamagata, Y., Nakamura, K., Ohashi, A. & Harada, H. Fluorescence in situ hybridization using 16S rRNA-targeted oligonucleotides reveals localization of methanogens and selected uncultured bacteria in mesophilic and thermophilic sludge granules. Appl. Environ. Microbiol. 65, 1280–1288 (1999).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Tawfik, A., Ohashi, A. & Harada, H. Sewage treatment in a combined up-flow anaerobic sludge blanket (UASB)-down-flow hanging sponge (DHS) system. Biochem. Eng. J. 29, 210–219 (2006).CAS 
Article 

Google Scholar 
Onodera, T. et al. Development of a sixth-generation down-flow hanging sponge (DHS) reactor using rigid sponge media for post-treatment of UASB treating municipal sewage. Bioresour. Technol. 152, 93–100 (2014).CAS 
PubMed 
Article 

Google Scholar 
Tandukar, M., Ohashi, A. & Harada, H. Performance comparison of a pilot-scale UASB and DHS system and activated sludge process for the treatment of municipal wastewater. Water Res. 41, 2697–2705 (2007).CAS 
PubMed 
Article 

Google Scholar 
Hallam, S. J. et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305, 1457–1462 (2004).CAS 
PubMed 
Article 

Google Scholar 
Nauhaus, K., Albrecht, M., Elvert, M., Boetius, A. & Widdel, F. In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. Environ. Microbiol. 9, 187–196 (2007).CAS 
PubMed 
Article 

Google Scholar 
Wegener, G., Niemann, H., Elvert, M., Hinrichs, K. & Boetius, A. Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane. Environ. Microbiol. 10, 2287–2298 (2008).CAS 
PubMed 
Article 

Google Scholar 
Hu, H., Natarajan, V. P. & Wang, F. Towards enriching and isolation of uncultivated archaea from marine sediments using a refined combination of conventional microbial cultivation methods. Mar. Life Sci. Technol. 3, 231–242 (2021).Article 
CAS 

Google Scholar 
Balch, W. E., Fox, G. E., Magrum, L. J., Woese, C. R. & Wolfe, R. S. Methanogens: reevaluation of a unique biological group. Microbiol. Rev. 43, 260–296 (1979).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Yokooji, Y. et al. Pantoate kinase and phosphopantothenate synthetase, two novel enzymes necessary for CoA biosynthesis in the Archaea. J. Biol. Chem. 284, 28137–28145 (2009).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Moench, T. & Zeikus, J. G. An improved preparation method for a titanium (III) media reductant. J. Microbiol. Methods 1, 199–202 (1983).CAS 
Article 

Google Scholar 
Miyashita, A. et al. Development of 16S rRNA gene-targeted primers for detection of archaeal anaerobic methanotrophs (ANMEs). FEMS Microbiol. Lett. 297, 31–37 (2009).CAS 
PubMed 
Article 

Google Scholar 
Sekiguchi, Y. et al. Sequence-specific cleavage of 16S rRNA for rapid and quantitative detection of particular groups of anaerobes in bioreactors. Water Sci. Technol. 52, 107–113 (2005).CAS 
PubMed 
Article 

Google Scholar 
Meechan, P. J. & Wilson, C. Use of ultraviolet lights in biological safety cabinets: a contrarian view. Appl. Biosaf. 11, 222–227 (2006).Article 

Google Scholar 
Imachi, H., Sekiguchi, Y., Kamagata, Y., Ohashi, A. & Harada, H. Cultivation and in situ detection of a thermophilic bacterium capable of oxidizing propionate in syntrophic association with hydrogenotrophic methanogens in a thermophilic methanogenic granular sludge. Appl. Environ. Microbiol. 66, 3608–3615 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Stams, A. J., Grolle, K. C., Frijters, C. T. & van Lier, J. B. Enrichment of thermophilic propionate-oxidizing bacteria in syntrophy with Methanobacterium thermoautotrophicum or Methanobacterium thermoformicicum. Appl. Environ. Microbiol. 58, 346–352 (1992).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Uchino, Y. & Suzuki, K. A simple preparation of liquid media for the cultivation of strict anaerobes. J. Pet. Environ. Biotechnol. S3, 001 (2011).
Google Scholar 
Akinyemi, T. S., Shao, N. & Whitman, W. B. Genus Methanothrix. In Bergey’s Manual of Systematics of Archaea and Bacteria (John Wiley & Sons, 2020). More

Deli, J., Matus, Z. & Tóth, G. Carotenoid composition in the fruits of asparagus officinalis. J. Agric. Food Chem. 48, 2793–2796 (2000).CAS 
PubMed 

Google Scholar 
Howard, L. R., Talcott, S. T., Brenes, C. H. & Villalon, B. Changes in phytochemical and antioxidant activity of selected pepper cultivars (Capsicum species) as influenced by maturity. J. Agric. Food Chem. 48, 1713–1720 (2000).CAS 
PubMed 

Google Scholar 
Odgerel, B. & Tserendulam, D. Effect of Chlorella as a biofertilizer on germination of wheat and barley grains. P. Mongolian Acad. Sci. 56(4), 26–31 (2016).
Google Scholar 
Sun, R. B., Guo, X. S., Wang, D. Z. & Chua, H. Y. Effects of long-term application of chemical and organic fertilizers on the abundance of microbial communities involved in the nitrogen cycle. Appl. Soil Ecol. 95(6), 171–178 (2015).
Google Scholar 
Yu, Y. Q., Luo, Z. B., Fu, H. & Jin, Y. Effect of balanced nutrient fertilizer: A case study in Pinggu District, Beijing China. Sci. Total Environ. 754, 1–8 (2021).
Google Scholar 
Ahmad, P. et al. Role of transgenic plants in agriculture and biopharming. Biotech. Adv. 30, 524–540 (2012).CAS 

Google Scholar 
Sherlock, R. & Morrey, J. D. Ethical Issues in Biotechnology (Rowman and Littlefield. Publishers, Inc., 2002).
Google Scholar 
Schiavon, M., Ertani, A. & Nardi, S. Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of TCA cycle and N metabolism in Zea mays L. J. Agric. Food Chem. 56, 11800–11808 (2008).CAS 
PubMed 

Google Scholar 
Muscolo, A., Sidari, M. & Nardi, S. Humic substance: relationship between structure and activity. Deeper information suggests univocal findings. J. Geochem. Explor. 129, 57–63 (2013).CAS 

Google Scholar 
Nardi, S., Carletti, P., Pizzeghello, D., Muscolo, A. Biological activities of humic substances. In Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems. PART I. Fundamentals and Impact of Mineral-Organic-Biota Interactions on the Formation, Transformation, Turnover, and Storage of Natural Nonliving Organic Matter (NOM). (Ed. Senesi, N., Xing, B., Huang, P.M.) 301–335 (John Wiley and Sons, Hoboken, 2009).Ertani, A., Nardi, S. & Altissimo, A. Review: long-term research activity on the biostimulant properties of natural origin compounds. Acta Hort. 1009, 181–188 (2013).
Google Scholar 
Ertani, A. et al. Biostimulant activity of two protein hydrolysates on the growth and nitrogen metabolism in maize seedlings. J. Plant Nutr. Soil Sci. 172, 237–244 (2009).CAS 

Google Scholar 
Vaccaro, S. et al. Effect of a compost and its water-soluble fractions on key enzymes of nitrogen metabolism in maize seedlings. J. Agric. Food Chem. 57, 11267–11276 (2009).CAS 
PubMed 

Google Scholar 
Azcona, I. et al. Growth and development of pepper are affected by humic substances derived from composted sludge. J. Plant Nutr. Soil Sci. 174, 916–924 (2011).CAS 

Google Scholar 
Schiavon, M. et al. High molecular size humic substances enhance phenylpropanoid metabolism in maize (Zea mays L.). J. Chem. Ecol. 36, 662–669 (2010).CAS 
PubMed 

Google Scholar 
Ertani, A., Schiavon, M., Muscolo, A. & Nardi, S. Alfalfa plant-derived biostimulant stimulates short-term growth of salt stressed Zea mays L. plants. Plant Soil 364, 145–158 (2013).CAS 

Google Scholar 
Pascual, I., Azcona, I., Morales, F., Aguirreolea, J. & Sanchez-Diaz, M. Growth, yield and physiology of verticillium-inoculated pepper plants treated with ATAD and composted sewage sludge. Plant Soil 319, 291–306 (2009).CAS 

Google Scholar 
Pascual, I. et al. Growth, yield and fruit quality of pepper plants amended with two sanitized sewage sludges. J. Agric. Food Chem. 58, 6951–6959 (2010).CAS 
PubMed 

Google Scholar 
Kim, M. J., Shim, C. K., Kim, Y. K., Ko, B. G. & Kim, B. H. Effect of Biostimulator Chlorella fusca on improving growth and qualities of Chinese Chives and Spinach in organic farm. Plant Pathol. J. 34(6), 567–574 (2018).CAS 
PubMed 
PubMed Central 

Google Scholar 
Pulz, O. & Gross, W. Valuable products from biotechnology of microalgae. Appl. Microbiol. Biot. 65, 635–648 (2004).CAS 

Google Scholar 
Kim, S. J., Ko, E. J., Hong, J. K. & Jeun, Y. C. Ultrastructures of Colletotrichum orbiculare in cucumber leaves expressing systemic acquired resistance mediated by Chlorella fusca. Plant Pathol. J. 34(2), 113–120 (2018).CAS 
PubMed 
PubMed Central 

Google Scholar 
Faheed, F. A. & Abd-El Fattah, Z. Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of Lettuce Plant. J. Agri. Soc. Sci. 4, 165–169 (2008).
Google Scholar 
Agwa, O. K., Ogugbue, C. J. & Williams, E. E. Field evidence of Chlorella vulgaris potentials as a biofertilizer for Hibiscus esculentus. Int. J. Agric. Res. 12(4), 181–189 (2017).CAS 

Google Scholar 
Ördög, V. et al. Screening microalgae for some potentially useful agricultural and pharmaceutical secondary metabolites. J. Appl. Physicol. 16, 309–401 (2004).
Google Scholar 
Stirk, W. A., Novák, O., Strnad, M. & van Staden, J. Cytokinins in macroalgae. Plant Growth Regul. 41, 13–24 (2003).CAS 

Google Scholar 
Kholssi, R., Marks, E. A. N., Montero, J. M. O., Debdoubi, A. & Rad, C. Biofertilizing effect of Chlorella sorokiniana suspensions on wheat growth. J. Plant Growth Regul. 38, 644–649 (2019).CAS 

Google Scholar 
Stirk, W. A., Ördög, V., Van Staden, J. & Jäger, K. Cytokinin-and auxin-like activity in Cyanophyta and microalgae. J. Appl. Phycol. 14, 215–221 (2002).CAS 

Google Scholar 
Park, E. R., Jo, J. O., Kim, S. M., Lee, M. Y. & Kim, K. S. Volatile flavor component of leek (Allium tuberosum Rotter). J. Korean Soc. Food Sci. Nutr. 27, 563–567 (1998) ((in Korean)).CAS 

Google Scholar 
Jin, H. et al. Ultrahigh-cell-density heterotrophic cultivation of the unicellular green microalga Scenedesmus acuminatus and application of the cells to photoautotrophic culture enhance biomass and lipid production. Biotechnol. Bioeng. 117, 96–108 (2020).CAS 
PubMed 

Google Scholar 
Kim, M. J., Shim, C. K., Kim, Y. K., Hong, S. J. & Kim, S. C. Isolation and morphological identification of fresh water green algae from organic farming habitats in Korea. Korean J. Org. Agric. 22, 743–760 (2014).
Google Scholar 
Li, L., Tian, S. L., Jiang, J. & Wang, Y. Regulation of nitric oxide to Capsicum under lower light intensities. S. Afr. J. Bot. 132, 268–276 (2020).CAS 

Google Scholar 
Cho, Y. Y., Oh, S. B., Oh, M. M. & Son, J. E. Estimation of individual leaf area, fresh weight, and dry weight of hydroponically grown cucumbers (Cucumis sativus L.) using leaf length, width, and SPAD value. Sci. Hortic-Amst. 111, 330–334 (2007).
Google Scholar 
Oster, U., Tanaka, R., Tanaka, A. & Rudiger, W. Cloning and functional expression of gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J. 21(3), 305–310 (2000).CAS 
PubMed 

Google Scholar 
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72(1–2), 248–254 (1976).CAS 
PubMed 

Google Scholar  More

Mack, R. N. et al. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689–710 (2000).
Google Scholar 
Turbelin, A. J., Malamud, B. D. & Francis, R. A. Mapping the global state of invasive alien species: Patterns of invasion and policy responses. Glob. Ecol. Biogeogr. 26, 78–92 (2017).
Google Scholar 
Jackson, M. C. Interactions among multiple invasive animals. Ecology 96, 2035–2041 (2015).CAS 
PubMed 

Google Scholar 
Rodriguez, L. F. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol. Invasions 8, 927–939 (2006).
Google Scholar 
Duenas, M. A. et al. The role played by invasive species in interactions with endangered and threatened species in the United States: A systematic review. Biodivers. Conserv. 27, 3171–3183 (2018).
Google Scholar 
Weidenhamer, J. D. & Callaway, R. M. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J. Chem. Ecol. 36, 59–69 (2010).CAS 
PubMed 

Google Scholar 
Bajwa, A. A., Chauhan, B. S., Farooq, M., Shabbir, A. & Adkins, S. W. What do we really know about alien plant invasion? A review of the invasion mechanism of one of the world’s worst weeds. Planta 244, 39–57 (2016).CAS 
PubMed 

Google Scholar 
Tallamy, D. W., Narango, D. L. & Mitchell, A. B. Do non-native plants contribute to insect declines?. Ecol. Entomol. 46, 729–742. https://doi.org/10.1111/een.12973 (2021).Article 

Google Scholar 
Bezemer, T. M., Harvey, J. A. & Cronin, J. T. Response of native insect communities to invasive plants. Annu. Rev. Entomol. 59, 119 (2014).CAS 
PubMed 

Google Scholar 
Cheng, F. & Cheng, Z. Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Front. Plant Sci. 6, 1020 (2015).PubMed 
PubMed Central 

Google Scholar 
Kalisz, S., Kivlin, S. N. & Bialic-Murphy, L. Allelopathy is pervasive in invasive plants. Biol. Invasions 23, 367–371 (2021).
Google Scholar 
Pyšek, P. et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species’ traits and environment. Glob. Change Biol. 18, 1725–1737 (2012).ADS 

Google Scholar 
Zhang, P., Li, B., Wu, J. & Hu, S. Invasive plants differentially affect soil biota through litter and rhizosphere pathways: A meta-analysis. Ecol. Lett. 22, 200–210 (2019).ADS 
PubMed 

Google Scholar 
Dudareva, N., Klempien, A., Muhlemann, J. K. & Kaplan, I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 198, 16–32 (2013).CAS 
PubMed 

Google Scholar 
Clavijo McCormick, A. Can plant–natural enemy communication withstand disruption by biotic and abiotic factors?. Ecol. Evol. 6, 8569–8582 (2016).PubMed 
PubMed Central 

Google Scholar 
Bruce, T. J., Wadhams, L. J. & Woodcock, C. M. Insect host location: A volatile situation. Trends Plant Sci. 10, 269–274 (2005).CAS 
PubMed 

Google Scholar 
Clavijo McCormick, A., Unsicker, S. B. & Gershenzon, J. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 17, 303–310 (2012).CAS 
PubMed 

Google Scholar 
Baldwin, I. T., Halitschke, R., Paschold, A., Von Dahl, C. C. & Preston, C. A. Volatile signaling in plant–plant interactions: “Talking trees” in the genomics era. Science 311, 812–815 (2006).ADS 
CAS 
PubMed 

Google Scholar 
Kegge, W. & Pierik, R. Biogenic volatile organic compounds and plant competition. Trends Plant Sci. 15, 126–132 (2010).CAS 
PubMed 

Google Scholar 
Effah, E., Holopainen, J. K. & Clavijo McCormick, A. Potential roles of volatile organic compounds in plant competition. Perspect. Plant Ecol. Evol. Syst. 38, 58–63 (2019).
Google Scholar 
Kigathi, R. N., Weisser, W. W., Reichelt, M., Gershenzon, J. & Unsicker, S. B. Plant volatile emission depends on the species composition of the neighboring plant community. BMC Plant Biol. 19, 1–17 (2019).
Google Scholar 
Karban, R., Wetzel, W. C., Shiojiri, K., Pezzola, E. & Blande, J. D. Geographic dialects in volatile communication between sagebrush individuals. Ecology 97, 2917–2924 (2016).PubMed 

Google Scholar 
Wheeler, G. S., David, A. S. & Lake, E. C. Volatile chemistry, not phylogeny, predicts host range of a biological control agent of Old-World climbing fern. Biol. Control 159, 104636 (2021).CAS 

Google Scholar 
Li, N. et al. Manipulating two olfactory cues causes a biological control beetle to shift to non-target plant species. J. Ecol. 105, 1534–1546 (2017).CAS 

Google Scholar 
Buddenhagen, C. E. Broom Control Monitoring at Tongariro National Park (Department of Conservation Wellington, 2000).
Google Scholar 
Hayes, L. et al. Biocontrol of Weeds: Achievements to Date and Future Outlook. Ecosystem services in New Zealand-conditions and trends Vol. 2, 375–385 (Manaaki Whenua Press, 2013).
Google Scholar 
Bagnall, A. Heather at Tongariro. A study of a weed introduction. Tussock Grasslands Mt. Lands Inst. Rev 41, 17–21 (1982).
Google Scholar 
Chapman, H. M. & Bannister, P. The spread of heather, Calluna vulgaris (L.) Hull, into indigenous plant communities of Tongariro National Park. N. Z. J. Ecol. 7–16 (1990).Effah, E. et al. Effects of two invasive weeds on arthropod community structure on the Central Plateau of New Zealand. Plants 9, 919 (2020).CAS 
PubMed Central 

Google Scholar 
Keesing, V. F. Impacts of invasion on community structure: habitat and invertebrate assemblage responses to Calluna vulgaris (L.) Hull invasion, in Tongariro National Park, New Zealand, Massey University Palmerston North, New Zealand, (1995).Peterson, P. G., Fowler, S. V. & Barrett, P. Is the poor establishment and performance of heather beetle in Tongariro National Park due to the impact of parasitoids predators or disease. N. Z. Plant Prot. 57, 89–93. https://doi.org/10.30843/nzpp.2004.57.6977 (2004).Article 

Google Scholar 
Ajpark. The brands and the bees: trade marks and the mānuka challenge for honey businesses, https://www.ajpark.com/insights/the-brands-and-the-bees-trade-marks-and-the-manuka-challenge-for-honey-businesses/#:~:text=M%C4%81nuka%20is%20a%20taonga%20species,may%20be%20offensive%20to%20M%C4%81ori (2021).Effah, E. et al. Seasonal and environmental variation in volatile emissions of the New Zealand native plant Leptospermum scoparium in weed-invaded and non-invaded sites. Sci. Rep. 10, 1–11 (2020).
Google Scholar 
Effah, E., Min Tun, K., Rangiwananga, N. & Clavijo McCormick, A. Mānuka clones differ in their volatile profiles: Potential implications for plant defence, pollinator attraction and bee products. Agronomy 12, 169 (2022).CAS 

Google Scholar 
Effah, E. et al. Natural variation in volatile emissions of the invasive weed Calluna vulgaris in New Zealand. Plants 9, 283 (2020).CAS 
PubMed Central 

Google Scholar 
Team, R. C. R: A language and environment for statistical computing (R Foundation for Statistical Computing, 2021).Ripley, B. et al. Package ‘mass’. Cran r 538, 113–120 (2013).
Google Scholar 
Chen, B. M., Liao, H. X., Chen, W. B., Wei, H. J. & Peng, S. L. Role of allelopathy in plant invasion and control of invasive plants. Allelopathy J 41, 155–166 (2017).
Google Scholar 
Ninkovic, V., Markovic, D. & Rensing, M. Plant volatiles as cues and signals in plant communication. Plant Cell Environ. 44, 1030–1043 (2021).CAS 
PubMed 

Google Scholar 
Holopainen, J. K. Multiple functions of inducible plant volatiles. Trends Plant Sci. 9, 529–533 (2004).CAS 
PubMed 

Google Scholar 
Rhoades, D. F. Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In Plant Resistance to Insects (ed. Hedin, P. A.) 55–68 (American Chemical Society, 1983).
Google Scholar 
Hedin, P. A. Plant Resistance to Insects (American Chemical Society, 1983).
Google Scholar 
Heil, M. & Karban, R. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25, 137–144 (2010).PubMed 

Google Scholar 
Barbosa, P. et al. Associational resistance and associational susceptibility: Having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40, 1 (2009).
Google Scholar 
Kigathi, R. N., Weisser, W. W., Veit, D., Gershenzon, J. & Unsicker, S. B. Plants suppress their emission of volatiles when growing with conspecifics. J. Chem. Ecol. 39, 537–545 (2013).CAS 
PubMed 

Google Scholar 
Peñuelas, J. & Llusià, J. Influence of intra-and inter-specific interference on terpene emission by Pinus halepensis and Quercus ilex seedlings. Biol. Plant. 41, 139–143 (1998).
Google Scholar 
Ormeno, E., Fernandez, C. & Mévy, J.-P. Plant coexistence alters terpene emission and content of Mediterranean species. Phytochemistry 68, 840–852 (2007).CAS 
PubMed 

Google Scholar 
Himanen, S. J. et al. Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants—A mechanism for associational herbivore resistance?. New Phytol. 186, 722–732 (2010).CAS 
PubMed 

Google Scholar 
Kessler, A. & Kalske, A. Plant secondary metabolite diversity and species interactions. Annu. Rev. Ecol. Evol. Syst. 49, 115–138 (2018).
Google Scholar 
Quintana-Rodriguez, E. et al. Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J. Ecol. 103, 250–260 (2015).CAS 

Google Scholar 
Loreto, F. & D’Auria, S. How do plants sense volatiles sent by other plants? Trends Plant Sci. (2021).Giordano, D., Facchiano, A., D’Auria, S. & Loreto, F. A hypothesis on the capacity of plant odorant-binding proteins to bind volatile isoprenoids based on in silico evidences. Elife 10, e66741 (2021).CAS 
PubMed 
PubMed Central 

Google Scholar 
Ninkovic, V., Markovic, D. & Dahlin, I. Decoding neighbour volatiles in preparation for future competition and implications for tritrophic interactions. Perspect. Plant Ecol. Evol. Syst. 23, 11–17 (2016).
Google Scholar 
Kegge, W. et al. Red: far-red light conditions affect the emission of volatile organic compounds from barley (Hordeum vulgare), leading to altered biomass allocation in neighbouring plants. Ann. Bot. 115, 961–970 (2015).CAS 
PubMed 
PubMed Central 

Google Scholar 
Gershenzon, J. Metabolic costs of terpenoid accumulation in higher plants. J. Chem. Ecol. 20, 1281–1328 (1994).CAS 
PubMed 

Google Scholar 
Anderson, P., Sadek, M., Larsson, M., Hansson, B. & Thöming, G. Larval host plant experience modulates both mate finding and oviposition choice in a moth. Anim. Behav. 85, 1169–1175 (2013).
Google Scholar 
Cunningham, J. P., Moore, C. J., Zalucki, M. P. & West, S. A. Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207, 87–94 (2004).PubMed 

Google Scholar 
McCormick, A. C., Reinecke, A., Gershenzon, J. & Unsicker, S. B. Feeding experience affects the behavioral response of polyphagous gypsy moth caterpillars to herbivore-induced poplar volatiles. J. Chem. Ecol. 42, 382–393 (2016).CAS 
PubMed 
PubMed Central 

Google Scholar 
Proffit, M., Khallaf, M. A., Carrasco, D., Larsson, M. C. & Anderson, P. ‘Do you remember the first time?’ Host plant preference in a moth is modulated by experiences during larval feeding and adult mating. Ecol. Lett. 18, 365–374 (2015).PubMed 

Google Scholar 
Mayhew, P. J. Herbivore host choice and optimal bad motherhood. Trends Ecol. Evol. 16, 165–167 (2001).PubMed 

Google Scholar 
Jackson, T. et al. Anticipating the unexpected–managing pasture pest outbreaks after large-scale land conversion (New Zealand Grassland Association, 2012).Townsend, R. J., Dunbar, J. E. & Jackson, T. A. Flight behaviour of the manuka chafers, Pyronota festiva (Fabricius) and Pyronota setosa (Given) (Coleoptera: Melolonthinae), on the flipped soils of Cape Foulwind on the West Coast of New Zealand. N. Z. Plant Prot. 71, 255–261. https://doi.org/10.30843/nzpp.2018.71.175 (2018).Article 

Google Scholar 
Ferguson, C. M. et al. Quantifying the economic cost of invertebrate pests to New Zealand’s pastoral industry. N. Z. J. Agric. Res. 62, 255–315 (2019).
Google Scholar 
Cunningham, J. Can mechanism help explain insect host choice?. J. Evol. Biol. 25, 244–251 (2012).CAS 
PubMed 

Google Scholar 
Syrett, P., Smith, L. A., Bourner, T. C., Fowler, S. V. & Wilcox, A. A European pest to control a New Zealand weed: Investigating the safety of heather beetle, Lochmaea suturalis (Coleoptera: Chrysomelidae) for biological control of heather, Calluna vulgaris. Bull. Entomol. Res. 90, 169–178. https://doi.org/10.1017/S0007485300000286 (2000).CAS 
Article 
PubMed 

Google Scholar 
Fowler, S., Harman, H., Memmott, J., Peterson, P. & Smith, L. In Proceedings of the XII International Symposium on Biological Control of Weeds (eds Julien, M. H. et al.) 495–502.Fowler, S. V. et al. Investigating the poor performance of heather beetle, Lochmaea suturalis (Thompson) (Coleoptera: Chrysomelidae), as a weed biocontrol agent in New Zealand: Has genetic bottlenecking resulted in small body size and poor winter survival?. Biol. Control 87, 32–38 (2015).
Google Scholar 
Effah, E. et al. Herbivory and attenuated UV radiation affect volatile emissions of the invasive weed Calluna vulgaris. Molecules 25, 3200 (2020).CAS 
PubMed Central 

Google Scholar 
Pearson, D. E. & Callaway, R. M. Indirect nontarget effects of host-specific biological control agents: Implications for biological control. Biol. Control 35, 288–298 (2005).
Google Scholar 
Rand, T. A. & Louda, S. M. Exotic weed invasion increases the susceptibility of native plants to attack by a biocontrol herbivore. Ecology 85, 1548–1554. https://doi.org/10.1890/03-3067 (2004).Article 

Google Scholar  More