Philippa Kaur

Site and sampling
We selected twelve monoculture tree stands of the most common tree species in Britain, Scots pine (Pinus sylvestris L.), Sitka spruce (Picea sitchensis Bong. Carr.), pedunculate oak (Quercus robur L.) and common beech (Fagus sylvatica L.). The majority of the stands were experimental sites within the Level II- ICP intensive forest monitoring network (http://icp-forests.net/), with the exception of Covert Wood, Shobdon and Goyt. The Goyt site was added as a high Ndep site as a contrast to the low Ndep Sitka spruce site in Scotland (Fig. 1, Table 1, Supplementary Table 1). For each species, forests were selected with similar soil type and age, but with contrasting Ndep, Sdep and climate, particularly rainfall and temperature, as described in Fig. 1, Table 1 and Supplementary Table 1. Stand information (mean tree height, mean diameter at the breast height and basal area) as measured for target years and for some of the forest stands are shown in Fig. S4.
At each ICP forest site, a plot of 0.25 ha was established in 1995 to carry out monitoring30 and a similar protocol was followed at the Goyt and Shobdon sites. Within each plot, 10 trees were selected for the collection of 3 wood cores per tree by using a 5 mm diameter increment borer, which were placed in paper straws for transport. Sampling was carried out between November 2010 and March 2011. Once in the laboratory, samples were dried at 70 °C for 48 h. Of the three wood cores sampled, one was kept for dendrochronology, with the other two used for stable isotope analyses.
Climate and atmospheric deposition data
Climate data (Temperature, T, Vapour Pressure Deficit, VPD, Precipitation, P) were obtained from automated weather stations at the sites and/or the nearest local meteorological stations (data were provided by the British Atmospheric Data Centre). Annual mean (Ta) and mean maximum (Tamax) values for temperature were calculated from monthly mean and maximum air temperature, T, respectively, and annual precipitation (Pa) was calculated as the sum of total monthly precipitations. Annual VPD was calculated from averaging monthly values obtained from mean monthly maximum temperature and minimum monthly relative humidity. For all the parameters, mean values were also calculated over the growing season, i.e., from May to September. We also considered the standardised precipitation-evapo-transpiration index, SPEI, relative to August, with 1 (SPEI8_1), 2 (SPEI8_2) and 3 (SPEI8_3) months time-scale and SPEI relative to December, with 1 and 12 months time-scale, the latter providing year-cumulated soil moisture conditions. SPEI values were obtained from the global database with 0.5 degrees spatial resolution available online at: https://sac.csic.es/spei/.
Yearly wet nitrogen (Ndep) and sulphur deposition (Sdep) were obtained from measured bulk precipitation and throughfall water volumes at the sites and measured elemental concentrations (NO3−, NH4+ and SO2–4) as previously described30. For the spatial analyses, we considered mean of annual deposition (sNdep and sSdep), obtained as the sum of total (NH4-N + NO3-N for Ndep) wet and dry deposition. The latter were estimated as difference between throughfall and bulk precipitation N fluxes30. For Rogate only 1 year (2010) of monitoring was available. For Goyt site, atmospheric deposition data collected at Ladybower were considered, as the two sites are 30 km apart. For two sites (i.e., Shobdon and Covert Wood), which were not part of the regular ICP forest sites, the wet deposition obtained from the UK 5 × 5 km grid Ndep and Sdep dataset was used4. The estimate included wet and dry NHx-N (NH4, NH3), NOy-N (NO2, NO3, HNO3) and S (SOx = SO2 and SO4) deposition, modelled using FRAME with 2005 emissions data4. However, only the total wet deposition was included in the analyses here, as we previously reported a good agreement between modelled and measured wet Ndep50.
For the temporal analyses, only wet deposition (as calculated from NO3−, NH4+ and SO2–4 concentrations in bulk precipitation) was considered (indicated as aNdep and aSdep), given the uncertainties associated with the quantification of the dry deposition. For instance, when differences between throughfall and bulk precipitation are  More

1.
Ruan, H., Zou, X., Scatena, F. & Zimmerman, J. Asynchronous fluctuation of soil microbial biomass and plant litterfall in a tropical wet forest. Plant Soil 260, 147–154 (2004).
CAS  Google Scholar 
2.
Ibekwe, A. M. et al. Impact of fumigants on soil microbial communities. Appl. Environ. Microbiol. 67, 3245–3257 (2001).
CAS  PubMed  PubMed Central  Google Scholar 

3.
Reiss, J., Bridle, J. R., Montoya, J. M. & Woodward, G. Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol. Evol. 24, 505–514 (2009).
PubMed  Google Scholar 

4.
Fuhrman, J. A. & Fuhrman, J. A. Microbial community structure and its functional implications. Nature 459, 193–199 (2009).
ADS  CAS  PubMed  Google Scholar 

5.
Lanzen, A. et al. Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci. Rep. 6, 28257. https://doi.org/10.1038/srep28257 (2016).
ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

6.
Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).
CAS  PubMed  Google Scholar 

7.
Oh, Y. M. et al. Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb. Ecol. 64, 1018–1027 (2012).
PubMed  Google Scholar 

8.
Walker, T. S., Bais, H. P., Grotewold, E. & Vivanco, J. M. Root exudation and rhizosphere biology. Plant Physiol. 132, 44–51 (2003).
CAS  PubMed  PubMed Central  Google Scholar 

9.
Herre, E. A. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466, 752–755 (2010).
ADS  PubMed  Google Scholar 

10.
Philippot, L., Raaijmakers, J. M., Lemanceau, P. & Wh, V. D. P. Going back to the roots: The microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013).
CAS  PubMed  Google Scholar 

11.
Hackl, E., Pfeffer, M., Donat, C., Bachmann, G. & Zechmeister-Boltenstern, S. Composition of the microbial communities in the mineral soil under different types of natural forest. Soil Biol. Biochem. 37, 661–671 (2005).
CAS  Google Scholar 

12.
Park, S. et al. Principal component analysis and discriminant analysis (PCA–DA) for discriminating profiles of terminal restriction fragment length polymorphism (T-RFLP) in soil bacterial communities. Soil Biol. Biochem. 38, 2344–2349 (2006).
CAS  Google Scholar 

13.
Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011).
ADS  CAS  PubMed  Google Scholar 

14.
Klimeš, L. Alpine plant life. Functional plant ecology of high mountain ecosystems by C. Körner. Folia Geobot. 41, 454–455 (2006).
Google Scholar 

15.
Diaz, H. F., Grosjean, M. & Graumlich, L. Climate variability and change in high elevation regions: Past, present and future. Clim. Change 59, 1–4 (2003).
Google Scholar 

16.
Schinner, F. & Gstraunthaler, G. Adaptation of microbial activities to the environmental conditions in alpine soils. Oecologia 50, 113–116 (1981).
ADS  PubMed  Google Scholar 

17.
Cui, H.-J. et al. Soil microbial community composition and its driving factors in alpine grasslands along a mountain elevational gradient. J. Mt. Sci. 13, 1013–1023. https://doi.org/10.1007/s11629-015-3614-7 (2016).
Article  Google Scholar 

18.
Zhang, B., Liang, C., He, H. & Zhang, X. Variations in soil microbial communities and residues along an altitude gradient on the northern slope of changbai mountain, china. PLoS ONE 8, e66184 (2013).
ADS  CAS  PubMed  PubMed Central  Google Scholar 

19.
Collins, C. G., Carey, C. J., Aronson, E. L., Kopp, C. W. & Diez, J. M. Direct and indirect effects of native range expansion on soil microbial community structure and function. J. Ecol. 104, 1271–1283 (2016).
Google Scholar 

20.
Margesin, R., Jud, M., Tscherko, D. & Schinner, F. Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol. Ecol. 67, 208–218 (2009).
CAS  PubMed  Google Scholar 

21.
Fierer, N. & Mcculley, R. L. Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342, 621–624 (2013).
ADS  CAS  PubMed  Google Scholar 

22.
Shi, Y. et al. Multi-scale variability analysis reveals the importance of spatial distance in shaping Arctic soil microbial functional communities. Soil Biol. Biochem. 86, 126–134 (2015).
CAS  Google Scholar 

23.
Yang, Y. et al. The microbial gene diversity along an elevation gradient of the Tibetan grassland. Isme J. Multidiscipl. J. Microb. Ecol. 8, 430–440 (2013).
Google Scholar 

24.
Ding, J. et al. Integrated metagenomics and network analysis of soil microbial community of the forest timberline. Sci. Rep. 5, 7994 (2015).
CAS  PubMed  PubMed Central  Google Scholar 

25.
Liu, J. et al. High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biol. Biochem. 70, 113–122 (2014).
CAS  Google Scholar 

26.
Brockett, B. F. T., Prescott, C. E. & Grayston, S. J. Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol. Biochem. 44, 9–20 (2012).
CAS  Google Scholar 

27.
Uroz, S., Tech, J. J., Sawaya, N. A., Frey-Klett, P. & Leveau, J. H. J. Structure and function of bacterial communities in ageing soils: Insights from the Mendocino ecological staircase. Soil Biol. Biochem. 69, 265–274 (2014).
CAS  Google Scholar 

28.
Shi, Y. et al. Vegetation-associated impacts on arctic tundra bacterial and microeukaryotic communities. Appl. Environ. Microbiol. 81, 492–501 (2014).
PubMed  Google Scholar 

29.
Zeglin, L. H. & Myrold, D. D. Fate of decomposed fungal cell wall material in organic horizons of old-growth douglas-fir forest soils. Soil Sci. Soc. Am. J. 77, 489–500 (2013).
ADS  CAS  Google Scholar 

30.
Wallander, H., Göransson, H. & Rosengren, U. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139, 89–97 (2004).
ADS  PubMed  Google Scholar 

31.
Colpaert, J. V., Laere, A. V. & Assche, J. A. V. Carbon and nitrogen allocation in ectomycorrhizal and non-mycorrhizal Pinus sylvestris L. seedlings. Tree Physiol. 16, 787–793 (1996).
CAS  PubMed  Google Scholar 

32.
Zhang, M. et al. Distribution of soil organic carbon fractions along the altitudinal gradient in Changbai mountain, China. Pedosphere 21, 615–620 (2011).
CAS  Google Scholar 

33.
Wenduo, X. U., Xingyuan, H. E., Chen, W. & Liu, C. Characteristics and succession rules of vegetation types in Changbai mountain. Chin. J. Ecol. 23, 162–174 (2004).
Google Scholar 

34.
Mao, Y., Yannarell, A. C., Davis, S. C. & Mackie, R. I. Impact of different bioenergy crops on N-cycling bacterial and archaeal communities in soil. Environ. Microbiol. 15, 928–942 (2012).
PubMed  Google Scholar 

35.
Grayston, S. J. et al. Assessing shifts in microbial community structure across a range of grasslands of differing management intensity using CLPP, PLFA and community DNA techniques. Appl. Soil. Ecol. 25, 63–84 (2004).
Google Scholar 

36.
Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120 (2009).
CAS  PubMed  PubMed Central  Google Scholar 

37.
Tedersoo, L. et al. Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol. Ecol. 21, 4160–4170 (2012).
PubMed  Google Scholar 

38.
Davey, M. L., Heegaard, E., Halvorsen, R., Kauserud, H. & Ohlson, M. Amplicon-pyrosequencing-based detection of compositional shifts in bryophyte-associated fungal communities along an elevation gradient. Mol. Ecol. 22, 368–383 (2013).
CAS  PubMed  Google Scholar 

39.
Mao, Y., Yannarell, A. C. & Mackie, R. I. Changes in N-transforming archaea and bacteria in soil during the establishment of bioenergy crops. PLoS ONE 6, e24750 (2011).
ADS  CAS  PubMed  PubMed Central  Google Scholar 

40.
Heijden, M. G. A. V. D., Bardgett, R. D. & Straalen, N. M. V. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).
PubMed  Google Scholar 

41.
Steltzer, H. & Bowman, W. D. Original articles: Differential influence of plant species on soil nitrogen transformations within moist meadow alpine Tundra. Ecosystems 1, 464–474 (1998).
CAS  Google Scholar 

42.
Shen, C., Ni, Y., Liang, W., Wang, J. & Chu, H. Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front. Microbiol. 6, 538–541 (2014).
CAS  Google Scholar 

43.
Zhang, C., Liu, G. B., Xue, S. & Xiao, L. Effect of different vegetation types on the rhizosphere soil microbial community structure in the loess plateau of China. J. Integr. Agric. 12, 2103–2113 (2013).
Google Scholar 

44.
Weand, M. P., Arthur, M. A., Lovett, G. M., Mcculley, R. L. & Weathers, K. C. Effects of tree species and N additions on forest floor microbial communities and extracellular enzyme activities. Soil Biol. Biochem. 42, 2161–2173 (2010).
CAS  Google Scholar 

45.
Wu, Z. et al. Terminal restriction fragment length polymorphism analysis of soil bacterial communities under different vegetation types in subtropical area. PLoS ONE https://doi.org/10.1371/journal.pone.0129397 (2015).
Article  PubMed  PubMed Central  Google Scholar 

46.
Singh, D. et al. Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol. Biochem. 68, 140–149 (2014).
ADS  CAS  Google Scholar 

47.
Fallen, M. Linking water and nutrients through the vadose zone: A fungal interface between the soil and plant systems. J. Arid Land 206, 155–163 (2011).
Google Scholar 

48.
Grayston, S. J., Griffith, G. S., Mawdsley, J. L., Campbell, C. D. & Bardgett, R. D. Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol. Biochem. 33, 533–551 (2001).
CAS  Google Scholar 

49.
Studies, R. Forest floor properties across sharp compositional boundaries separating trembling aspen and jack pine stands in the southern boreal forest. Plant Soil 345, 353–364 (2011).
Google Scholar 

50.
Ruzicka, S., Edgerton, D., Norman, M. & Hill, T. The utility of ergosterol as a bioindicator of fungi in temperate soils. Soil Biol. Biochem. 32, 989–1005 (2000).
CAS  Google Scholar 

51.
Weete, J. D., Abril, M. & Blackwell, M. Phylogenetic distribution of fungal sterols. PLoS ONE 5, e10899 (2010).
ADS  PubMed  PubMed Central  Google Scholar 

52.
Shen, C. et al. Dramatic increases of soil microbial functional gene diversity at the treeline ecotone of Changbai mountain. Front. Microbiol. https://doi.org/10.3389/fmicb.2016.01184 (2016).
Article  PubMed  PubMed Central  Google Scholar 

53.
Quideau, S. A., Chadwick, O. A., Benesi, A., Graham, R. C. & Anderson, M. A. A direct link between forest vegetation type and soil organic matter composition. Geoderma 104, 41–60 (2001).
ADS  CAS  Google Scholar 

54.
Tian, J. et al. Linkages between the soil organic matter fractions and the microbial metabolic functional diversity within a broad-leaved Korean pine forest. Eur. J. Soil Biol. 66, 57–64 (2015).
CAS  Google Scholar 

55.
Yuan, Y., Si, G., Jian, W., Luo, T. & Zhang, G. Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan plateau. FEMS Microbiol. Ecol. 87, 121–132 (2013).
PubMed  Google Scholar 

56.
Fierer, N. et al. Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92, 797–804 (2011).
PubMed  Google Scholar 

57.
Shen, C., Ni, Y., Liang, W., Wang, J. & Chu, H. Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front. Microbiol. 6, 582. https://doi.org/10.3389/fmicb.2015.00582 (2015).
Article  PubMed  PubMed Central  Google Scholar 

58.
Hinsinger, P., Bengough, A. G., Vetterlein, D. & Young, I. M. Rhizosphere: Biophysics, biogeochemistry and ecological relevance. Plant Soil 321, 117–152 (2009).
CAS  Google Scholar 

59.
Shen, C. et al. Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95, 3190–3202 (2014).
Google Scholar 

60.
Jarvis, S. G., Woodward, S. & Taylor, A. F. S. Strong altitudinal partitioning in the distributions of ectomycorrhizal fungi along a short (300 m) elevation gradient. New Phytol. 206, 1145–1155 (2015).
CAS  PubMed  Google Scholar 

61.
Lanzén, A. et al. Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci. Rep. 6, 28257 (2016).
ADS  PubMed  PubMed Central  Google Scholar 

62.
Shen, C. et al. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai mountain. Soil Biol. Biochem. 57, 204–211 (2013).
CAS  Google Scholar 

63.
Siles, J. A. & Margesin, R. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors?. Microb. Ecol. 72, 207–220 (2016).
PubMed  PubMed Central  Google Scholar 

64.
Sagovamareckova, M., Cermak, L., Omelka, M., Kyselkova, M. & Kopecky, J. Bacterial diversity and abundance of a creek valleysites reflected soil pH and season. Open Life Sci. https://doi.org/10.1515/biol-2015-0007 (2015).
Article  Google Scholar 

65.
Smith, J. L., Halvorson, J. J. & Bolton, H. Soil properties and microbial activity across a 500m elevation gradient in a semi-arid environment. Soil Biol. Biochem. 34, 1749–1757 (2002).
CAS  Google Scholar 

66.
Yergeau, E., Kang, S., He, Z., Zhou, J. & Kowalchuk, G. A. Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J. 1, 163–179 (2007).
CAS  PubMed  Google Scholar 

67.
Kai, X. et al. Warming alters expressions of microbial functional genes important to ecosystem functioning. Front. Microbiol. 7, 668 (2016).
ADS  Google Scholar 

68.
Jing, C. et al. Available nitrogen is the key factor influencing soil microbial functional gene diversity in tropical rainforest. BMC Microbiol. 15, 397–398 (2015).
Google Scholar 

69.
Griffiths, R. I. et al. The bacterial biogeography of British soils. Environ. Microbiol. 13, 1642–1654 (2011).
PubMed  Google Scholar 

70.
Davey, M. L., Nybakken, L., Kauserud, H. & Ohlson, M. Fungal biomass associated with the phyllosphere of bryophytes and vascular plants. Mycol. Res. 113, 1254–1260 (2009).
CAS  PubMed  Google Scholar 

71.
Meier, C. L., Rapp, J., Bowers, R. M., Silman, M. & Fierer, N. Fungal growth on a common wood substrate across a tropical elevation gradient: Temperature sensitivity, community composition, and potential for above-ground decomposition. Soil Biol. Biochem. 42, 1083–1090 (2010).
CAS  Google Scholar 

72.
Tu, S., Sun, J., Guo, Z. & Gu, F. On relationship between root exudates and plant nutrition in rhizosphere. Soil Environ. 9, 64–67 (2000).
Google Scholar 

73.
Zhang, C., Liu, G., Xue, S. & Song, Z. Rhizosphere soil microbial activity under different vegetation types on the Loess Plateau, China. Geoderma 161, 115–125 (2011).
ADS  CAS  Google Scholar 

74.
Zeng, S., Zhiyao, S. U., Chen, B. & Yuanchun, Y. U. A review on the rhizosphere nutrition ecology research. J. Nanjing For. Univ. 27, 79 (2003).
Google Scholar 

75.
Wei, Z., Xiaojuan, Q. I., Jianwei, L., Zhengxiang, Y. U. & Xia, C. Characterization of microbial community structure in rhizosphere soils of cowskin Azalea (Rhododendron aureum Georgi) on northern slope of Changbai mountains, China. Chin. Geogr. Sci. 26, 78–89 (2016).
Google Scholar 

76.
Yang, X. & Wu, G. The strategy for conservation and sustainable utilization of biodiversity in Changbaishan biosphere reserve. J. For. Res. 9, 217–222 (1998).
Google Scholar 

77.
Zong, S. et al. Analysis of the process and impacts of Deyeuxia angustifolia invasion on the Alpine Tundra, Changbai mountain. Acta Ecol. Sin. 34, 87–104 (2014).
Google Scholar 

78.
Batten, K. M., Scow, K. M., Davies, K. F. & Harrison, S. P. Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol. Invas. 8, 217–230 (2006).
Google Scholar 

79.
Mebius, L. J. A rapid method for the determination of organic carbon in soil. Anal. Chim. Acta 22, 120–124 (1960).
CAS  Google Scholar 

80.
Industry, D. I. Design in industry. Electr. Power 28, 228–228 (1982).
Google Scholar 

81.
Murphy, J. & Riley, J. P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962).
CAS  Google Scholar 

82.
Brookes, P. C., Landman, A., Pruden, G. & Jenkinson, D. S. Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17, 837–842 (1985).
CAS  Google Scholar 

83.
Schinner, F. & Mersi, W. V. Xylanase-, CM-cellulase- and invertase activity in soil: An improved method. Soil Biol. Biochem. 22, 511–515 (1990).
CAS  Google Scholar 

84.
Johnson, J. L. & Temple, K. L. Some variables affecting the measurement of “catalase activity” in Soil1. Soil Sci. Soc. Am. J. 28, 207–209 (1964).
ADS  CAS  Google Scholar 

85.
Klose, S. & Tabatabai, M. A. Urease activity of microbial biomass in soils as affected by cropping systems. Biol. Fertil. Soils 31, 191–199 (2000).
CAS  Google Scholar 

86.
Vaughan, D. & Ord, B. G. An effect of soil organic matter on invertase activity in soil. Soil Biol. Biochem. 12, 449–450 (1980).
CAS  Google Scholar 

87.
Djajakirana, G., Joergensen, R. G. & Meyer, B. Ergosterol and microbial biomass relationship in soil. Biol. Fertil. Soils 22, 299–304 (1996).
CAS  Google Scholar 

88.
Levy-Booth, D. J., Prescott, C. E. & Grayston, S. J. Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol. Biochem. 75, 11–25 (2014).
CAS  Google Scholar 

89.
Yuan, H. et al. Abundance and composition of CO_2 fixating bacteria in relation to long-term fertilization of paddy soils. Acta Ecol. Sin. 32, 183–189 (2012).
CAS  Google Scholar 

90.
Chen, J., Yu, Z., Michel, F. C. Jr., Wittum, T. & Morrison, M. Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Appl. Environ. Microbiol. 73, 4407–4416. https://doi.org/10.1128/AEM.02799-06 (2007).
CAS  Article  PubMed  PubMed Central  Google Scholar 

91.
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998 (2013).
CAS  PubMed  Google Scholar 

92.
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).
CAS  PubMed  Google Scholar 

93.
Maidak, B. L. et al. The ribosomal database project (RDP). Nucleic Acids Res. 24, 82–85 (1996).
CAS  PubMed  PubMed Central  Google Scholar 

94.
CoreTeam, R. R: A language and environment for statistical computing. (2013).

95.
Oksanen, B. J., Kindt, R., Legendre, P. & O’Hara, B. vegan: Community Ecology Package. R package version 1.8-6 (accessed 10 December 2019); https://CRAN.R-project.org/package=vegan.

96.
Oksanen, J. et al. vegan: Community ecology package. R package version 1.17-3. J. Stat. Softw. 48, 103–132 (2010).
Google Scholar 

97.
Nd, S. A., Potvin, L. R. & Lilleskov, E. A. Fertility-dependent effects of ectomycorrhizal fungal communities on white spruce seedling nutrition. Mycorrhiza 25, 649–662 (2015).
Google Scholar 

98.
Arbuckle, J. L. Amos 7.0 User’s Guide. (SPSS, 2006). More

1.
Panizzi, A. R. Economic importance of stink bugs (Pentatomidae). In Heteroptera of economic importance (eds Schaefer, C. W. & Panizzi, A. R.) 421–474 (CRC Press, Boca Ratón, 2000).
Google Scholar 
2.
Akin, S., Phillips, J. & Johnson, D.T. Biology, identification and management of the redbanded stink bug. Arkansas, US Cooperative Extension Service, University of Arkansas, U.S. Dept. of Agriculture, and county governments cooperating. FSA7078 (2011).

3.
Corrêa-Ferreira, B. S. & Azevedo, J. Soybean seed damage by diferente species of stink bugs. Agric. For. Entomol. 4, 145–150 (2002).
Google Scholar 

4.
Panizzi, A. R. & Slansky, F. Jr. Review of phytophagous pentatomids (Hemiptera: Pentatomidae) associated with soybean in the Americas. Fla. Entomol. 68, 184–203 (1985).
Google Scholar 

5.
Zerbino, M. S. & Panizzi, A. R. The underestimated role of pest pentatomid parasitoids in Southern South America. Arth. Plant Int. 13, 703–718 (2019).
Google Scholar 

6.
Panizzi, A. R. & Corrêa-Ferreira, B. S. Dynamics in the insect fauna adaptation to soybean in the tropics. Trends Entomol. 1, 71–88 (1997).
Google Scholar 

7.
Gomes, E. C., Hayashida, R. & Bueno, A. F. Dichelops melacanthus and Euschistus heros injury on maize: Basis for re-evaluating stink bug thresholds for IPM decisions. Crop Prot. 130, 105050 (2020).
CAS  Google Scholar 

8.
Smaniotto, L. F. & Panizzi, A. R. Interactions of selected species of stink bugs (Hemiptera: Heteroptera: Pentatomidae) from leguminous crops with plants in the Neotropics. Florida Entomol. 98, 7–17 (2015).
Google Scholar 

9.
Bueno, A. F., Bortolotto, O. C., Pomari-Fernandes, A. & França-Neto, J. B. Assessment of a more conservative stink bug economic threshold for managing stink bugs in Brazilian soybean. Crop Prot. 71, 132–137 (2015).
Google Scholar 

10.
Sosa-Gómez, D.R., Corso, I.C. & Morales, L. Insecticide resistance to endosulfan, monocrotophos and methamidophos in the neotropical brown stink bug, Euschistus heros (F.) Neotrop. Entomol. 30, 317–320 (2001).

11.
Sosa-Gómez, D. R. & Silva, J. J. D. Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná Brazil. Pesq. Agrop. Bras 45, 767–769 (2010).
Google Scholar 

12.
Bueno, A. F. et al. Effects of integrated pest management, biological control and prophylactic use of insecticides on the management and sustainability of soybean. Crop Prot. 30, 937–945 (2011).
Google Scholar 

13.
van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J. & Urbaneja, A. Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63, 39–59 (2018).
Google Scholar 

14.
Koppel, A. L., Herbert, D. A. Jr., Kuhar, T. P. & Kamminga, K. Survey of stink bug (Hemiptera: Pentatomidae) egg parasitoids in wheat, soybean, and vegetable crops in southeast Virginia. Environ. Entomol. 38, 375–379 (2009).
CAS  PubMed  Google Scholar 

15.
Laumann, R. A. et al. Egg parasitoid wasps as natural enemies of the Neotropical stink bug Dichelops melacanthus. Pesq. Agropec. Bras. 45, 442–449 (2010).
Google Scholar 

16.
Corrêa-Ferreira, B. S. & Moscardi, F. Seasonal occurrence and host spectrum of egg parasitoids associated with soybean stink bugs. Biol. Control. 5, 196–202 (1995).
Google Scholar 

17.
Cividanes, F. J. Development and emergence of Trissolcus brochymenae (Ashmead) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae) at different temperatures. An. Soc. Entomol. Bras. 25, 207–211 (1996).
Google Scholar 

18.
Silva, G. V., Bueno, A. F., Neves, P. M. O. J. & Favetti, B. M. Biological characteristics and parasitism capacity of Telenomus podisi (Hymenoptera: Platygastridae) on eggs of Euschistus heros (Hemiptera: Pentatomidae). J. Agric. Sci. 10, 210–220 (2018).
Google Scholar 

19.
Laumann, R. A. et al. Comparative biology and functional response of Trissolcus spp. (Hymenoptera: Scelionidae) and implications for stink bugs (Hemiptera: Pentatomidae) biological control. Biol. Control. 44, 32–41 (2008).
Google Scholar 

20.
Favetti, B. M., Krinski, D., Butnariu, A. R. & Loiácono, M. S. Egg parasitoids of Edessa meditabunda (Fabricius) (Pentatomidae) in lettuce crop. Rev. Bras. Entomol. 57, 236–237 (2013).
Google Scholar 

21.
Margaría, C. B., Loiácono, M. S. & Lanteri, A. A. New geographic and host records for scelionid wasps (Hymenoptera: Scelionidae) parasitoids of insect pests in South America. Zootaxa 2314, 41–49 (2009).
Google Scholar 

22.
Peres, W. A. A. & Corrêa-Ferreira, B. S. Methodology of mass multiplication of Telenomus podisi Ashmead and Trissolcus basalis (Hymenoptera: Scelionidae) on eggs of Euschistus heros (Hemiptera: Pentatomidae). Neotrop. Entomol. 33, 457–462 (2004).
Google Scholar 

23.
Panizzi, A. R., Parra, J. R. P., Santos, C. H. & Carvalho, D. R. Rearing the southern green stink bug using artificial dry diet and artificial plant. Pesq. Agropec. Bras. 35, 1709–1715 (2000).
Google Scholar 

24.
Thuler, R. T., Volpe, H. X. L., Bortoli, S. A., Goulart, R. M. & Viana, C. L. T. Metodologia para avaliação da preferência hospedeira de parasitoides do gênero Trichogramma Westood. Bol. San. Veg. 33, 333–340 (2007).
Google Scholar 

25.
Queiroz, A. P., Taguti, E. A., Bueno, A. F., Grande, M. L. M. & Costa, C. O. Host preferences of Telenomus podisi (Hymenoptera: Scelionidae): parasitism on eggs of Dichelops melacanthus, Euschistus heros, and Podisus nigrispinus (Hemiptera: Pentatomidae). Neotrop. Entomol. 47, 543–552 (2018).
CAS  PubMed  Google Scholar 

26.
van Lenteren, J. C. Quality control and production of biological control agents: theory and testing procedures 327 (CABI, Wallingford, 2003).
Google Scholar 

27.
Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).
MathSciNet  MATH  Google Scholar 

28.
Burr, I. W. & Foster, L. A. A Test for Equality of Variances (University of Purdue, West Lafayette, 1972).
Google Scholar 

29.
Institute, S. A. S. SAS User’s Guide: Statistics, Version 8e (SAS Institute, Cary, NC, 2009).
Google Scholar 

30.
Sujii, E. R., Costa, M. L. M., Pires, C. S. S., Colazza, S. & Borges, M. Inter and intra-guild interactions in egg parasitoid species of the soybean stink bug complex. Pesq. Agropec. Bras. 37, 1541–1549 (2002).
Google Scholar 

31.
Zhou, Y., Abram, P. K., Boivin, G. & Brodeur, J. Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid. Entomol. Exp. Appl. 151, 106–111 (2014).
Google Scholar 

32.
Jones, T. S., Bilton, A. R., Mak, L. & Sait, S. M. Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecol. Evol. 5, 459–465 (2015).
PubMed  PubMed Central  Google Scholar 

33.
Orr, D. B. Scelionid wasps as biological control agents: a review. Florida Entomol. 71, 506–528 (1988).
Google Scholar 

34.
Blackiston, D. J., Casey, E. S. & Weiss, M. R. Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar?. PlosOne 3, e1736 (2008).
ADS  Google Scholar 

35.
Kaiser, L., Pham-Delegue, M. H. & Masson, C. Behavioural study of plasticity in host preferences of Trichogramma maidis (Hymenoptera: Trichogrammatidae). Physiol. Entomol. 14, 53–60 (1989).
Google Scholar 

36.
Gandolfi, M., Mattiacci, L. & Dorn, S. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. Lond. B 270, 2623–2629 (2003).
Google Scholar 

37.
Corbet, S. A. Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Entomol. 10, 143–153 (1985).
Google Scholar 

38.
Pluke, R. W. H. & Leibee, G. L. Host preferences of Trichogramma pretiosum and the influence of prior ovipositional experience on the parasitism of Plutella xylostella and Pseudoplusia includes eggs. Biocontrol 51, 569–583 (2006).
Google Scholar 

39.
Stephens, D. W. & Krebs, J. R. Foraging theory (Princeton University Press, Princeton, 1986).
Google Scholar 

40.
Vinson, S. B. & Iwantsch, G. F. Host suitability for insect parasitoids. Annu. Rev. Entomol. 25, 397–419 (1980).
Google Scholar 

41.
Bin, F., Vinson, S. B., Strand, M. R., Colazza, S. & Jones, W. A. Jr. Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol. Entomol. 18, 7–15 (1993).
Google Scholar 

42.
Borges, M. et al. Semiochemical and physical stimuli involved in host recognition by Telenomus podisi (Hymenoptera: Scelionidae) toward Euschistus heros (Heteroptera: Pentatomidae). Physiol. Entomol. 24, 227–233 (1999).
Google Scholar 

43.
Borges, M. & Aldrich, J. R. Attractant pheromone for Nearctic stink bug, Euschistus obscurus (Heteroptera: Pentatomidae): insight in to a Neotropical relative. J. Chem. Ecol. 20, 1095–1102 (1994).
CAS  PubMed  Google Scholar 

44.
Pomari, A. F., Bueno, A. F., Bueno, R. C. O. F. & Menezes Junior, A. O. Biological Characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 105, 73–81 (2012).
Google Scholar 

45.
Bueno, R. C. O., Parra, J. R. P. & Bueno, A. F. Biological characteristics and thermal requirements of a Brazilian strain of the parasitoid Trichogramma pretiosum reared on eggs of Pseudoplusia includes and Anticarsia gemmatalis. Biol. Control. 51, 355–361 (2009).
Google Scholar 

46.
Cônsoli, F. L., Kitajima, E. W. & Parra, J. R. P. Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Int. J. Insect. Morphol. Embriol. 28, 211–229 (1999).
Google Scholar 

47.
Bai, B., Luck, R. F., Forster, L., Stephens, B. & Janssen, J. A. M. The effect of host size on quality attributes of the egg parasitoid Trichogramma pretiosum. Entomol. Exp. Appl. 64, 37–48 (1992).
Google Scholar 

48.
Schwartz, A. & Gerling, D. Adult biology of Telenomus remus (Hymenoptera: Scelionidae) under laboratory conditions. Entomophaga 19, 482–492 (1974).
Google Scholar 

49.
Charnov, E. L., Los-Den Hartogh, R. L., Jones, W. T. & Van Den Assem, J. Sex ratio evolution in a variable environment. Nature 289, 27–33 (1981).
ADS  CAS  PubMed  Google Scholar 

50.
Houseweart, M. W., Jennings, D. T., Welty, C. & Southard, S. G. Progeny production by Trichogramma minutum (Hymenoptera: Trichogrammatidae) utilizing eggs for Choristoneura fumiferana (Lepidoptera: Tortricidae) and Sitotroga cerealella (Lepidoptera: Gelechiidae). Can. Entomol. 115, 1245–1252 (1983).
Google Scholar 

51.
Sequeira, R. & Mackauer, M. Covariance of adult size and development time in the parasitoid wasp Aphidius ervi in relation to the size of its host Acyrthosiphon pisum. Evol. Ecol. 6, 34–44 (1992).
Google Scholar 

52.
Mackauer, M. Sexual size dimorphism in solitary wasps: influence of host quality. Oikos 76, 265–272 (1996).
Google Scholar  More

Verily Life Sciences, South San Francisco, CA, USA
Jacob E. Crawford, David W. Clarke, Victor Criswell, Mark Desnoyer, Kyle Gong, Kaycie C. Hopkins, Paul Howell, Justin S. Hyde, Josh Livni, Charlie Behling, Renzo Benza, Willa Chen, Craig Eldershaw, Daniel Greeley, Yi Han, Bridgette Hughes, Evdoxia Kakani, Joe Karbowski, Angus Kitchell, Erika Lee, Teresa Lin, Jianyi Liu, Martin Lozano, Warren MacDonald, Matty Metlitz, Sara N. Mitchell, David Moore, Johanna R. Ohm, Kathleen Parkes, Alexandra Porshnikoff, Chris Robuck, Martin Sheridan, Robert Sobecki, Peter Smith, Jessica Stevenson, Jordan Sullivan, Brian Wasson, Allison M. Weakley, Mark Wilhelm, Joshua Won, Ari Yasunaga, William C. Chan, Nigel Snoad, Linus Upson, Tiantian Zha, Peter Massaro & Bradley J. White

Consolidated Mosquito Abatement District, Parlier, CA, USA
Devon Cornel, Brittany Deegan, Jodi Holeman & F. Steven Mulligan

MosquitoMate Inc., Lexington, KY, USA
Karen L. Dobson, James W. Mains & Stephen L. Dobson

Department of Entomology, University of Kentucky, Lexington, KY, USA
Stephen L. Dobson More

Many Acropora corals at Scott Reef spawn biannually, but most individuals spawn either in autumn or in spring (not in both seasons) and are thus temporally isolated from one another with respect to reproduction10,25. Gametogenesis takes ~ 4 to 6 months in Acropora corals at Scott Reef10. While it is unknown whether gametogenesis occurs at different rates in the different seasons, coral colonies experience different environmental conditions through the gametogenic period, leading up to spawning in the spring and autumn spawning seasons. Gametogenesis occurs through austral winter and early spring prior to the spring spawning (October/November), when water temperatures are cooler and days are shorter. Conversely, gametogenesis occurs through summer prior to the autumn spawning (March/April), when water temperatures are warmest (potentially stressfully warm), the days are longest, and tropical cyclones occur. Both spring and autumn spawning correspond with seasonal minimums in wind speed26,27. Within the thermal tolerance limits of the coral, warmer water temperatures and longer days theoretically increase energy availability for reproductive processes through increased metabolic activity and elevated photosynthesis28,29. Despite the different environmental conditions through gametogenesis, there were no seasonal differences in fecundity and eggs size observed in the biannually spawning Acropora corals studied here. There are several possibilities for the lack of seasonality observed in reproductive output. Firstly, fecundity and egg size varied widely within species, which confounded inferences about whether reproductive output was higher in a particular season. Other studies have similarly reported high variability, particularly in fecundity. Fecundity can vary widely with season22,30 and between years31, but there is also high variation between colonies, within a single colony22, with colony age30 and between colonies at different depths13. Fecundity can also vary in response to stressors13, however, there was no evidence of environmental stress, such as damaging waves from cyclones or heat stress causing coral bleaching32, before or during the period when samples were collected for this study. Adaptive plasticity in egg size (in response to conditions parents are exposed to), is discussed further below. Secondly, Scott Reef is situated in the tropics (14°S) with relatively small seasonal variations in temperature and day length, and has a light regime that is affected by high cloud cover during the summer cyclone season. Water temperatures are 2–4 °C cooler in the winter months leading up to spring spawning than in the summer months prior to autumn spawning. Day length is 1–2 h shorter in winter compared to summer, however summer cyclones and rainfall mean that overall sunshine hours are higher in the winter months. Consequently, there are cooler temperatures with more sunshine hours in the months leading to the spring spawning and warmer temperatures with less sunshine hours in the months leading to the autumn spawning, which may result in comparable available energy for reproduction during both spawning events. Thirdly, seasonal differences in environmental conditions may indeed drive some seasonal differences in energetics, but these could be channeled into other life history processes, such as calcification12,33, rather than fecundity and egg size. Variation in available energy may also affect egg quality rather than size or number. For example, in other invertebrates (greenlip abalone), while the size of the eggs do not increase, the density of protein and lipids increase throughout the spawning season34 and may indicate an increase in the quality over size of the egg. However, a study on the reef-building coral Montipora capitata, reported stable egg quality (lipids and antioxidants) regardless of the environmental conditions the parent colonies were exposed to, although egg sizes were not presented in this work35. The higher polyp fecundity in spring observed in A. microclados may have been an adaptive response to cooler (less favourable) conditions in spring. That is, an increase in parental investment to increase survival in less favourable conditions36. Alternatively, more sunshine hours during winter gametogenesis may have provided additional energy to produce more eggs in this species.
Early work on egg size and number of eggs suggests a simple trade-off model. That is, assuming resources for reproduction are limited, then an increase in gamete size should result in a reduction in the number of gametes37. Correspondingly, earlier studies of different coral species, genera and morphologies reported an inverse relationship between coral egg sizes and the number of eggs (fecundity)21,22,23, also suggesting that energy is channelled to either fewer large eggs or many small eggs19,20. However, in these cases, the reductions in fecundity with egg size among genera were attributed to the differences in polyp morphology (and sometimes reproductive mode i.e. brooder vs spawner). That is, differences in polyp size and structure can also affect egg size and fecundity38,39 independently of energetics. In our between species comparison, we did not see an inverse relationship between egg size and number of eggs (Fig. 3), but there were also no large differences in corallite size for the seven Acropora species studied here (see Supplementary Table S4 for corallite sizes of our species). However, it is important to note that the differences in reproductive mode and morphology (including polyp structure and size) between genera and species, interferes with the egg size versus number of eggs comparison in the context of a trade-off model. In order to determine if there is a trade-off between egg size and number of eggs, we need to look at individuals within a species. That is, do individuals with large eggs have fewer eggs than individuals with smaller eggs of the same species? We have been unable to locate any other dataset providing a within species comparison. Our study demonstrates that there is no direct relationship between egg size and fecundity, within these species of Acropora, and suggests that there is more than just a simple trade-off in resources influencing these measures.
Egg size has been shown to be a phenotypically plastic trait, regulated by the conditions the parent colony is exposed to. For example, a study on the broadcast spawning ascidian, Styela plicata, demonstrated that parents maintained at high densities produced smaller eggs, presumably reflecting the higher sperm concentrations expected at high adult densities, and therefore reduced requirement for a large target40. While the study was unable to measure the number of gametes, and provide an egg size versus number of eggs comparison, it did suggest that egg size is an adaptive plastic response, rather than a simple energetic constraint. Several studies have also reported varying effects of stress on the number and size of eggs. Under temperature stress sufficient to cause bleaching, corals within the same species can produce either fewer eggs (and maintain size) or smaller eggs (and maintain numbers) depending on their zooxanthellae clade and lipid levels15. Corals exposed to elevated nutrients levels also adjusted their reproductive output, with nitrogen reducing both egg size and number of eggs, and phosphorus producing smaller, but more eggs41. Furthermore, when coral colonies are transplanted to different latitudes, they adjust their egg size to be similar to local colonies. A transplant study conducted in Taiwan reported that coral colonies transplanted to higher latitudes and cooler waters, developed larger eggs, similar to local colonies, as an increased investment response to unfavourable conditions36. This phenotypic plasticity may allow for a type of maternal ‘bet-hedging’, where parents increase within clutch variation in offspring phenotype in response to unpredictable environmental conditions42. The results of our study showed high within species natural variability, but this variability was not consistent with the trade-off model. That is, while there may have been both large and small mature eggs within a species, the large eggs did not necessarily correspond with fewer eggs in a polyp. Within species size variation amongst offspring has traditionally been underestimated43, however, since offspring size can affect dispersal potential, producing a range of sizes, could spread offspring through a range of habitats, thereby spreading the risk of reproductive failure44.
It is often assumed that if resources are limited for reproduction, then an increase in egg size should result in a reduction in the number of eggs37. However, there are no datasets directly comparing egg size and number within coral species. We have shown that in seven Acropora coral species this trade-off between size and number did not occur. We also did not see any seasonal differences in these measures. We recorded high natural variability in both mature egg size and fecundity, a factor that should not be overlooked when using these measures to gauge or compare reproductive output (e.g. between seasons, years, locations). Since egg size and fecundity are affected by parent colony energy reserves, energy allocation to a range of other life history processes (e.g. growth and repair), polyp size and morphology, responses to environmental conditions, and the interaction of these factors, it is unlikely that there is a simple trade-off between size and number of eggs. It is also unlikely that these measures are constrained only by energetics, given the adaptive phenotypic plasticity reported in other studies36, 40. Furthermore, parental investment can come in the form of increased egg quality (e.g. lipids or antioxidants), rather than size or number of eggs. More research into coral energetics, natural variability, and adaptive plasticity is required to determine the mechanisms behind some of the patterns we observed, but our study doesn’t support a simple trade-off model in coral reproduction. More

1.
Edenhofer, O. Climate Change 2014: Mitigation of Climate Change (Cambridge University Press, Cambridge, 2015).
Google Scholar 
2.
Grassi, G. et al. The key role of forests in meeting climate targets requires science for credible mitigation. Nat. Clim. Change 7, 220–226 (2017).
ADS  Article  Google Scholar 

3.
Duarte, C. M., Losada, I. J., Hendriks, I. E., Mazarrasa, I. & Marbà, N. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Change 3, 961–968 (2013).
ADS  CAS  Article  Google Scholar 

4.
Mcleod, E. et al. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO 2. Front. Ecol. Environ. 9, 552–560 (2011).
Article  Google Scholar 

5.
Alongi, D. M. Carbon cycling and storage in mangrove forests. Ann. Rev. Mar. Sci. 6, 195–219 (2014).
Article  Google Scholar 

6.
Macreadie, P. I. et al. The future of Blue Carbon science. Nat. Commun. 10, 3998 (2019).
ADS  Article  Google Scholar 

7.
Wernberg, T., Krumhansl, K., Filbee-Dexter, K. & Pedersen, M. Status and trends for the world’s kelp forests. In World Seas: An Environmental Evaluation (ed. Sheppard, C.) 57–78 (Elsevier, London, UK, 2019).

8.
Krause-Jensen, D. et al. Sequestration of macroalgal carbon: the elephant in the Blue Carbon room. Biol. Lett. 14, 20180236 (2018).
Article  Google Scholar 

9.
Howard, J. et al. Clarifying the role of coastal and marine systems in climate mitigation. Front. Ecol. Environ. 15, 42–50 (2017).
Article  Google Scholar 

10.
Krumhansl, K. & Scheibling, R. Production and fate of kelp detritus. Mar. Ecol. Prog. Ser. 467, 281–302 (2012).
ADS  Article  Google Scholar 

11.
Hill, R. et al. Can macroalgae contribute to blue carbon? An Australian perspective. Limnol. Oceanogr. 60, 1689–1706 (2015).
ADS  CAS  Article  Google Scholar 

12.
Ortega, A. et al. Important contribution of macroalgae to oceanic carbon sequestration. Nat. Geosci. 12, 748–754 (2019).
ADS  CAS  Article  Google Scholar 

13.
Wernberg, T. & Filbee-Dexter, K. Missing the marine forest for the trees. Mar. Ecol. Prog. Ser. 612, 209–215 (2019).
ADS  Article  Google Scholar 

14.
Filbee-Dexter, K., Feehan, C. J. & Scheibling, R. E. Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Mar. Ecol. Prog. Ser. 543, 141–152 (2016).
ADS  CAS  Article  Google Scholar 

15.
Smale, D. A., Moore, P. J., Queirós, A. M., Higgs, N. D. & Burrows, M. T. Appreciating interconnectivity between habitats is key to blue carbon management. Front. Ecol. Environ. 16, 71–73 (2018).
Article  Google Scholar 

16.
Filbee-Dexter, K., Wernberg, T., Ramirez-Llodra, E., Norderhaug, K. M. & Pedersen, M. F. Movement of pulsed resource subsidies from shallow kelp forests to deep fjords. Oecologia 187, 291–304 (2018).
ADS  Article  Google Scholar 

17.
Queirós, A. M. et al. Connected macroalgal-sediment systems: blue carbon and food webs in the deep coastal ocean. Ecol. Monogr. https://doi.org/10.1002/ecm.1366 (2019).
Article  Google Scholar 

18.
Kokubu, Y., Rothäusler, E., Filippi, J. B., Durieux, E. D. H. & Komatsu, T. Revealing the deposition of macrophytes transported offshore: evidence of their long-distance dispersal and seasonal aggregation to the deep sea. Sci. Rep. 9, 1–11 (2019).
CAS  Article  Google Scholar 

19.
Krause-Jensen, D. & Duarte, C. M. Substantial role of macroalgae in marine carbon sequestration. Nat. Geosci. 9, 737–742 (2016).
ADS  CAS  Article  Google Scholar 

20.
Bennett, S. et al. The ‘Great Southern Reef’: social, ecological and economic value of Australia’s neglected kelp forests. Mar. Freshw. Res. https://doi.org/10.1071/MF15232 (2016).
Article  Google Scholar 

21.
Serrano, O. et al. Australian vegetated coastal ecosystems as global hotspots for climate change mitigation. Nat. Commun. 10, 4313 (2019).
ADS  Article  Google Scholar 

22.
Fulton, C. J. et al. Sea temperature shapes seasonal fluctuations in seaweed biomass within the Ningaloo coral reef ecosystem. Limnol. Oceanogr. 59, 156–166 (2014).
ADS  Article  Google Scholar 

23.
Coleman, M. A. & Wernberg, T. Forgotten underwater forests: The key role of fucoids on Australian temperate reefs. Ecol. Evol. 7, 8406–8418 (2017).
Article  Google Scholar 

24.
Cresswell, A. K. et al. Translating local benthic community structure to national biogenic reef habitat types. Glob. Ecol. Biogeogr. 26, 1112–1125 (2017).
Article  Google Scholar 

25.
Kennedy, H. et al. Seagrass sediments as a global carbon sink: isotopic constraints. Glob. Biogeochem. Cycles 24, GB4026. https://doi.org/10.1029/2010GB003848 (2010).
ADS  CAS  Article  Google Scholar 

26.
Boyer, K. E. & Fong, P. Macroalgal-mediated transfers of water column nitrogen to intertidal sediments and salt marsh plants. J. Exp. Mar. Biol. Ecol. 321, 59–69 (2005).
CAS  Article  Google Scholar 

27.
Wernberg, T., Vanderklift, M. A., How, J. & Lavery, P. S. Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147, 692–701 (2006).
ADS  Article  Google Scholar 

28.
Spivak, A. C., Sanderman, J., Bowen, J. L., Canuel, E. A. & Hopkinson, C. S. Global-change controls on soil-carbon accumulation and loss in coastal vegetated ecosystems. Nat. Geosci. 12, 685–692 (2019).
ADS  CAS  Article  Google Scholar 

29.
Pedersen, M. F. et al. Detrital carbon production and export in high latitude kelp forests. Oecologia 1, 1–33. https://doi.org/10.1007/s00442-019-04573-z (2019).
Article  Google Scholar 

30.
Chew, S. T. & Gallagher, J. B. Accounting for black carbon lowers estimates of blue carbon storage services. Sci. Rep. 8, 2553 (2018).
ADS  Article  Google Scholar 

31.
Wernberg, T. et al. Biology and ecology of the globally significant kelp Ecklonia radiata. Mar. Biol. Annu. Rev. 57, 265–324 (2019).

32.
Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science (80-). 353, 169–172 (2016).
ADS  CAS  Article  Google Scholar 

33.
Connell, S. et al. Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 360, 63–72 (2008).
ADS  Article  Google Scholar 

34.
Gaylard, S. The Health of Subtidal Reefs Along the Adelaide Metropolitan Coastline 1996–99 (Environment Protection Authority, Carlton, 2003).
Google Scholar 

35.
Carnell, P. E. & Keough, M. J. Reconstructing historical marine populations reveals major decline of a kelp forest ecosystem in Australia. Estuaries Coasts 42, 765–778 (2019).
Article  Google Scholar 

36.
Ling, S. D., Johnson, C. R., Ridgeway, K., Hobday, A. J. & Haddon, M. Climate-driven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics. Glob. Change. Biol. 15, 719–731 (2009).
ADS  Article  Google Scholar 

37.
Ling, S. & Keane, J. Resurvey of the longspined sea urchin (Centrostephanus rodgersii) and associated barren reef in Tasmania. Technical Report, University of Tasmania, https://eprints.utas.edu.au/28761/ (2018).

38.
Vergés, A. et al. Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc. Natl. Acad. Sci. USA 113, 13791–13796 (2016).
Article  Google Scholar 

39.
Martínez, B. et al. Distribution models predict large contractions of habitat-forming seaweeds in response to ocean warming. Divers. Distrib. 24, 1350–1366 (2018).
Article  Google Scholar 

40.
Coleman, M. A., Wood, G., Filbee-Dexter, K., Minne, A. J. P., Goold, V. et al.. Restore or redefine: future trajectories for restoration. Front. Mar. Sci. 7, 237. https://doi.org/10.3389/fmars.2020.00237 (2020).
Article  Google Scholar 

41.
Layton, C., Coleman, M. A., Marzinelli, E. M., Steinberg, P. D., Swearer, S. E. et al. Kelp forest restoration in Australia. Front. Mar. Sci. 7, 237. https://doi.org/10.3389/fmars.2020.00074 (2020).
Article  Google Scholar 

42.
Fredriksen, S. et al. Green gravel: a novel restoration tool to combat kelp forest decline. Sci. Rep. 10, 1–7 (2020).
Article  Google Scholar 

43.
Marzinelli, E. M. et al. Large-scale geographic variation in distribution and abundance of Australian deep-water kelp forests. PLoS ONE 10, e0118390. https://doi.org/10.1371/journal.pone.0118390. (2015).
CAS  Article  PubMed  PubMed Central  Google Scholar 

44.
Connell, S. D. & Irving, A. D. Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia. J. Biogeogr. 35, 1608–1621 (2008).
Article  Google Scholar 

45.
Wernberg, T., Coleman, M., Fairhead, A., Miller, S. & Thomsen, M. Morphology of Ecklonia radiata (Phaeophyta: Laminarales) along its geographic distribution in south-western Australia and Australasia. Mar. Biol. 143, 47–55 (2003).
Article  Google Scholar 

46.
Staehr, P. A. & Wernberg, T. Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J. Phycol. 45, 91–99 (2009).
CAS  Article  Google Scholar  More

1.
Talbot, J. M. Grounds for Agreement. The Political Economy of the Coffee Commodity Chain 1–250 (Rowman & Little field Publishers Inc, Washington, DC, 2004).
Google Scholar 
2.
Igami, M. Market power in international commodity trade: The case of coffee. J. Ind. Econ. 63, 225–248 (2015).
Google Scholar 

3.
Waller, J. M., Bigger, M. & Hillocks, R. J. Coffee Pests, Diseases and their Management 1–400 (CABI, Wallingford, 2007).
Google Scholar 

4.
Sustainable Commodities Marketplace Series. Global Market Report: Coffee. International Institute for Sustainable Development (IISD). https://www.iisd.org/sites/default/files/publications/ssi-global-market-report-coffee.pdf (2019).

5.
Vega, F. E., Infante, F., Castillo, A. & Jaramillo, J. The coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera:Curculionidae): A short review, with recent findings and future research directions. Terr. Arthropod. Rev. 2, 129–147 (2009).
Google Scholar 

6.
Vega, F. E., Infante, F. & Johnson, A. J. In The Genus Hypothenemus, Biology and Ecology of Native and Invasive Species with Emphasis on H. hampei, The Coffee Berry Borer in Bark Beetles (eds Vega, F. E. & Hofstetter, R. W.) 427–494 (Elsevier, London, 2015).

7.
International Coffee Organization. IPM of Coffee Berry Borer (CFC/ICO/02). Impact Assessment. https://www.ico.org/project_pdfs/CBB_ICO02.pdf (2009).

8.
CABI. Stopping the coffee berry borer in its tracks. Development projects. https://www.cabi.org/uploads/projectsdb/documents/2734/Coffee-berry-borer_HR.pdf (2012).

9.
Burbano, E., Wright, M., Bright, D. E. & Vega, F. E. New record for the coffee berry borer, Hypothenemus hampei, in Hawaii. J. Insect. Sci. 11, 117 (2011).
PubMed  PubMed Central  Google Scholar 

10.
State of Hawaii Department of Agriculture. Coffee berry borer Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae). Hawaii Department of Agriculture. New Pest Advisory 10–01. https://hdoa.hawaii.gov/pi/files/2013/01/Hypothenemus-hampei-NPA-MASTER.pdf (2014).

11.
NAPPO. North American Plant Protection Organization. Detection of the coffee berry borer, Hypothenemus hampei, in Puerto Rico. Official Pest Alerts. https://www.pestalerts.org/es/official-pest-report/detecciones-de-la-broca-del-caf-hypothenemus-hampei-en-puerto-rico-estados (2007).

12.
Mariño, Y. A. et al. The coffee berry borer (Coleoptera: Curculionidae) in Puerto Rico: Distribution, infestation, and population per fruit. J. Insect Sci. 17(2), 58 (2017).
PubMed Central  Google Scholar 

13.
Wood, S. L. Bark and Ambrosia Beetles of South America. 1–900 (Monte L. Bean Sci. Mus., Provo, Utah, 2007).

14.
Damon, A. A review of the biology and control of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Bull. Entomol. Res. 90, 453–465 (2000).
CAS  PubMed  Google Scholar 

15.
Batchelor, T. P., Hardy, I. C. W. & Barrera, J. F. Interactions among bethylid parasitoid species attacking the coffee berry borer, Hypothenemus hampei (Coleoptera:Scolytidae). Biol. Control 36, 106–118 (2006).
Google Scholar 

16.
Benassi, V.L.R.M. Biologia em diferentes temperaturas e ocorrência de Prorops nasuta Wat. e Cephalonomia stephanoderis Betr. (Hymenoptera:Bethylidae) parasitando Hypothenemus hampei (Ferr.) (Coleoptera:Scolytidae). Biblioteca digital Brasileira de teses e dissertações, https://bdtd.ibict.br/vufind/Record/UNSP_921d283e6a2f9fc4271784147e404a27 (2007).

17.
Maldonado, C. E. & Benavides, P. Evaluación del establecimiento de Cephalonomia stephanoderis y Prorops nasuta, controladores de Hypothenemus hampei, en Colombia. Revista cenicafé (Colombia) 58, 333–339 (2007).
Google Scholar 

18.
Pérez-Lachaud, G., Batchelor, T. P. & Hardy, I. C. W. Wasp eat wasp: Facultative hyperparasitism and intra-guild predation by bethylid wasps. Biol. Control 30, 149–155 (2004).
Google Scholar 

19.
Gutierrez, A. P. & Baumgärtner, J. U. Multitrophic level models of predator-prey energetics: II: A realistic model of plant-herbivore-parasitoid-predator interactions. Can. Entomol. 116, 933–949 (1984).
Google Scholar 

20.
Gutierrez, A. P. Applied Population Ecology: A Supply-Demand Approach 1–300 (Wiley, Hoboken, 1996).
Google Scholar 

21.
Gutierrez, A. P., Villacorta, A., Cure, J. R. & Ellis, C. K. Tritrophic analysis of the coffee (Coffea arabica)-coffee berry borer Hypothenemus hampei (Ferrari)-parasitoid system. Anais da sociedade entomológica do brasil 27(3), 357–385 (1998).
Google Scholar 

22.
Rodríguez, D., Cure, J. R., Cotes, J. M., Gutierrez, A. P. & Cantor, F. A coffee agroecosystem model. I. Growth and development of the coffee plant. Ecol. Model. 222, 3626–3639 (2011).
Google Scholar 

23.
Rodríguez, D., Cure, J. R., Cotes, J. M., Gutierrez, A. P. & Cantor, F. A coffee agroecosystem model. II. Dynamics of coffee berry borer. Ecol. Model. 248, 203–214 (2013).
Google Scholar 

24.
Rodríguez, D., Cure, J. R., Cotes, J. M. & Gutierrez, A. P. A coffee agroecosystem model. III. Parasitoids of the coffee berry borer (Hypothenemus hampei). Ecol. Model. 363, 96–110 (2017).
Google Scholar 

25.
Arcila, J., Jaramillo, A., Baldión, V. & La Bustillo, A. E. floración del cafeto y su relación con el control de la broca. Avances Técnicos Cenicafé 193, 6 (1993).
Google Scholar 

26.
Vélez, B. E., Jaramillo, A., Cháves, B. & Franco, M. Distribución de la floración y la cosecha de café en tres altitudes. Avances Técnicos Cenicafé 272, 4 (2000).
Google Scholar 

27.
Benavides, P. & Arévalo, H. Manejo integrado: una estrategia para el control de la broca del café en Colombia. Revista Cenicafé (Colombia) 53(1), 39–48 (2002).
Google Scholar 

28.
Benavides, P., Bustillo, A. E., Cárdenas, M. R. & Montoya, E. C. Análisis biológico y económico del manejo integrado de la broca del café en Colombia. Revista Cenicafé (Colombia) 54(1), 5–23 (2003).
Google Scholar 

29.
Aristizábal, L. F., Jiménez, M., Bustillo, A. E. & Arthurs, S. P. Monitoring cultural control practices for coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) management in a small coffee farm in Colombia. Fla. Entomol. 94(3), 685–687 (2011).
Google Scholar 

30.
Aristizábal, L. F. Frequent and efficient harvesting practices to reduce coffee berry borer populations. CBB Notes Number 05, Kailua-Kona, Hawaii https://www.researchgate.net/publication/340502340_CBB_Notes_Frequent_and_Efficient_Harvesting_Practices_to_Reduce_Coffee_Berry_Borer_Populations (2020).

31.
Villalba, D. A., Bustillo, A. E. & Cháves, B. Evaluación de insecticidas para el control de la broca del café en Colombia. Revista Cenicafé (Colombia) 46(3), 152–163 (1995).
Google Scholar 

32.
Benavides, P., Bustillo, A. E., Montoya, E. C., Cárdenas, M. R. & Mejía, C. G. Participación del control cultural, químico y biológico en el manejo de la broca del café. Rev. Colomb. Entomol. 28, 161–165 (2002).
Google Scholar 

33.
Tabares, J. E., Villalba, D. A., Bustillo, A. E. & Vallejo, L. F. Eficacia de insecticidas para el control de la broca del café usando diferentes equipos de aspersión. Revista Cenicafé (Colombia) 59(3), 227–237 (2008).
Google Scholar 

34.
Beers, E. H. et al. Nontarget effect of orchard pesticides on natural enemies: Lessons from the field and the laboratory. Biol. Control 102, 44–52 (2016).
CAS  Google Scholar 

35.
Bueno, A. F., Carvalho, G. A., Santos, A. C., Sosa-Gómez, D. R. & Silva, D. M. Pesticide selectivity to natural enemies: Challenges and constrains for research and field recommendation. Ciência Rural (Santa María, Brasil) https://doi.org/10.1590/0103-8478cr20160829 (2017).
Article  Google Scholar 

36.
Klein, A. M., Steffan-Dewenter, I. & Tscharntke, T. Bee pollination and fruit set of Coffea arabica and C. canephora (Rubiaceae). Am. J. Bot. 90, 153–157 (2003).
PubMed  Google Scholar 

37.
Woodill, A. J., Nakamoto, S. T., Kawabata, A. M. & Leung, P. S. To spray or not to spray: A decision analysis of coffee berry borer in Hawaii. Insects 8(4), 116 (2017).
PubMed Central  Google Scholar 

38.
González, M. T., Posada, F. J. & Bustillo, A. E. Bioensayo para evaluar la patogenicidad de Beauveria bassiana (Bals.) Vuill. sobre la broca del café, Hypothenemus hampei (Ferrari). Rev. Colomb. Entomol. 19, 123–130 (1993).
Google Scholar 

39.
Tobar, S. P., Vélez, P. E. & Montoya, E. C. Evaluación en campo de un aislamiento del hongo Beauveria bassiana seleccionado por resistencia a la luz ultravioleta. Revista Cenicafé (Colombia) 50(3), 195–204 (1999).
Google Scholar 

40.
De la Rosa, W., Alatorre, R. R., Barrera, J. F. & Toriello, C. Effect of Beauveria bassiana and Metarhizium anisopliae (Deuteromycetes) upon the Coffee Berry Borer (Coleoptera: Scolytidae) under field conditions. J. Econ. Entomol. 93, 1409–1413 (2000).
PubMed  Google Scholar 

41.
Posada, F. J., Osorio, E. & Velásquez, E. T. Evaluación de la patogenicidad de Beauveria bassiana sobre la broca del café empleando el método de aspersión foliar. Rev. Colomb. Entomol. 28, 139–144 (2002).
Google Scholar 

42.
Cárdenas, A. B., Villalba, D. A., Bustillo, A. E., Montoya, E. C. & Góngora, C. E. Eficacia de mezclas de cepas del hongo Beauveria bassiana en el control de la broca del café. Revista Cenicafé (Colombia) 58, 293–303 (2007).
Google Scholar 

43.
Aristizábal, L. F. et al. Integrated pest management of coffee berry borer in Hawaii and Puerto Rico: Current status and prospects. Insects 8, 123 (2017).
PubMed Central  Google Scholar 

44.
Greco, B. E., Wright, M. G., Burgueño, J. & Jaronski, S. TEfficacy of Beauveria bassiana applications on coffee berry borer across an elevation gradient in Hawaii. Biocontrol Sci. Technol. 28, 995–1013 (2018).
Google Scholar 

45.
Hollingsworth, R. G. et al. Incorporating Beauveria bassiana into an integrated pest management plan for coffee berry borer in Hawaii. Front. Sustain. Food Syst. 4, 22 (2020).
Google Scholar 

46.
Bustillo, A. E. Una revisión sobre la broca del café, Hypothenemus hampei, en Colombia. Rev. Colomb. Entomol. 32(2), 101–116 (2006).
Google Scholar 

47.
Bustillo, A. E. El manejo de cafetales y su relación con el control de la broca del café en Colombia 2nd edn, 1–40 (Cenicafé, Chinchiná, 2007).
Google Scholar 

48.
Bernal, M. G., Bustillo, A. E. & Posada, F. J. Virulencia de aislamientos de Metarhizyum anisopliae y su eficacia en campo sobre Hypothenemus hampei. Rev. Colomb. Entomol. 20(4), 225–228 (1994).
Google Scholar 

49.
Molina, J. P. A. & López, N. J. C. Efeito da aplicação de nematoides entomopatogênicos sobre frutos infestados com broca-do-café, Hypothenemus hampei (Coleoptera:Scolytidae). Nematol. Bras. (Brazil) 33(2), 115–122 (2009).
Google Scholar 

50.
Benavides-Machado, P., Quintero, J. C. & López, J. C. Evaluación en el laboratorio de nematodos entomopatógenos nativos para el control de la broca del café. Cenicafé (Colombia) 61(2), 119–131 (2010).
Google Scholar 

51.
Guide, B. A. et al. Selection of entomopathogenic nematodes and evaluation of their compatibility with cyantraniliprole for the control of Hypothenemus hampei. Semina: Ciências Agrárias, Londrina 39(4), 1489–1502. https://doi.org/10.5433/1679-0359.2018v39n4p1489 (2018).
Article  Google Scholar 

52.
Lara, J. C., Lopez, J. N. & Bustillo, A. E. Efecto de entomonemátodos sobre poblaciones de la broca del café, Hypothenems hampei (Coleoptera, Scolytidae) en frutos en el suelo. Rev. Colomb. Entomol. 30(2), 179–185 (2004).
Google Scholar 

53.
Abraham, Y. J., Moore, D. & Goodwin, G. Rearing and aspects of biology of Cephalonomia stephanoderis and Prorops nasuta (Hymenoptera:Bethylidae) parasitoid of the coffee berry borer Hypothenemus hampei (Coleoptera: scolytidae). Bull. Entomol. Res. 80, 121–128 (1990).
Google Scholar 

54.
Barrera, J. F. Dynamique des populations du scolyte des fruits du caféier, Hypothenemus hampei (Coleoptera: Scolytidae), et lutte biologique avec le parasitoide Cephalonomia stephanoderis (Hymenoptera: Bethylidae), au Chiapas, Mexique. Ph.D. Thesis. Université Paul Sabatier, Toulouse III. France. https://agritrop.cirad.fr/312449/ (1994).

55.
Aristizábal, L. F., Baker, P. S., Orozco, H. J. & Orozco, G. L. Determinación de las horas del día convenientes para la liberación del parasitoide Cephalonomia stephanoderis (Betrem) (Hymenoptera: Bethylidae). Rev. Colomb. Entomol. 2, 99–104 (1996).
Google Scholar 

56.
Aristizábal, L. F., Baker, P. S., Orozco, S. J. & Chaves, B. Parasitismo de Cephalonomia stephanoderis Betrem sobre una población de Hypothenemus hampei (Ferrari) con niveles bajos de infestación en campo. Rev. Colomb. Entomol. 23, 157–164 (1997).
Google Scholar 

57.
Aristizábal, L. F., Bustillo, A. E., Baker, P. F., Orozco, H. J. & Chaves, C. B. Efecto depredador del parasitoide Cephalonomia stephanoderis (Hymenoptera: bethylidae) sobre los estados inmaduros de Hypothenemus hampei (Coleoptera: scolytidae) en condiciones de campo. Rev. Colomb. Entomol. 24, 35–41 (1998).
Google Scholar 

58.
Damon, A. & Valle, J. Comparison of two release techniques for the use of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), to control the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae) in Soconusco, southeastern Mexico. Biol. Control 24, 117–127 (2002).
Google Scholar 

59.
Hempel, A. Combate à broca do café por meio da Vespa de Uganda. Bol. Agric. Zoot. Vet. 6(9), 551–555 (1933).
Google Scholar 

60.
Hempel, A. A Prorops nasuta Waterston no Brasil. Arquivos do Instituto Biológico de São Paulo (Brasil) 5, 197–212 (1934).
Google Scholar 

61.
Infante, F. Biological Control of Hypothenemus hampei(Coleoptera:Scolytidae) in Mexico, Using the Parasitoid Prorops nasuta (Hymenoptera:bethylidae) Dissertation, Imperial College, University of London (1998).

62.
Infante, F. et al. Cría de Phymastichus coffea, parasitoide de la broca del café y algunas notas sobre su historia de vida. Southw. Entomol. 19, 313–315 (1994).
Google Scholar 

63.
Aristizábal, L. F., Salazar, H. M., Mejía, C. G. & Bustillo, A. E. Introducción y evaluación de Phymastichus coffea (Hymenoptera: eulophidae) en fincas de pequeños caficultores, a través de investigación participativa. Rev. Colomb. Entomol. 30, 219–234 (2004).
Google Scholar 

64.
Castillo, A., Infante, F., Vera-Graziano, J. & Trujillo, J. Host-discrimination by Phymastichus coffea, a parasitoid of the coffee berry borer (Coleoptera: Scolytidae). Biocontrol 49, 655–663 (2004).
Google Scholar 

65.
Castillo, A. et al. Laboratory parasitism by Phymastichus coffea (Hymenoptera: Eulophidae) upon non-target bark beetles associated with coffee plantations. Fla. Entomol. 87, 274–277 (2004).
Google Scholar 

66.
Castillo, A. Análisis Post-introductorio Del Parasitoide Africano Phymastichus coffea LaSalle (Hymenoptera: Eulophidae) a México. Dissertation 1–150 (Colegio de Postgraduados, Montecillo, Estado de México, 2005).

67.
Jaramillo, J., Bustillo, A. E., Montoya, E. C. & Borgemeister, C. Biological control of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae) by Phymastichus coffea (Hymenoptera: Eulophidae) in Colombia. Bull. Entomol. Res 95, 1–6 (2005).
Google Scholar 

68.
Jaramillo, J., Borgemeister, C. & Setamou, M. Field superparasitism by Phymastichus coffea, a parasitoid of adult coffee berry borer, Hypothenemus hampei. Entomol. Exp. Appl. 119, 231–237 (2006).
Google Scholar 

69.
Riaño, N., Arcila, J., Jaramillo, A. & Chaves, B. Acumulación de materia seca y extracción de nutrimentos por Coffea arabica L. cv. Colombia en tres localidades de la zona cafetera central. Revista Cenicafé (Colombia) 55, 265–276 (2004).
Google Scholar 

70.
CENICAFE Anuario Meteorológico Cafetero 1990–1995. Chinchiná, Colombia, https://books.google.com.co/books?id=6QNdAAAAMAAJ&hl=es&source=gbs_book_other_versions (Centro Nacional de Investigaciones del Café “Pedro Uribe Mejía”, 1995).

71.
Prescott, J. A. Evaporation from water Surface in relation to solar radiation. Trans. R. Soc. South. Aust. 64, 114–118 (1940).
Google Scholar 

72.
Baker, P.S. The Coffee Berry Borer in Colombia. Final report of the DFID-Cenicafé-CABI Bioscience IPM for coffee Project (CNTR 93/1536A), https://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=CAFE.xis&method=post&formato= 2&cantidad=1&expresion=mfn=019976 (Chinchiná, Colombia DFID-Cenicafé, 1999).

73.
Mejía, J. W., Bustillo, A. E., Orozco, H. J. & Cháves, B. Efecto de cuatro insecticidas y de Beauveria bassiana sobre Prorops nasuta (Hymenoptera:Bethylidae), parasitoide de la broca del café. Rev. Colomb. Entomol. 26(3–4), 117–123 (2000).
Google Scholar 

74.
McCullagh, P. & Nelder, J. A. Generalized Linear Models 1–532 (Chapman and Hall/CRC, Boca Raton, 1989) (ISBN 9780412317606).
Google Scholar 

75.
Lactin, D. J., Holliday, N. J., Johnson, D. L. & Craigen, R. Improved rate model of temperature dependent development by arthropods. Environ. Entomol. 24, 68–75 (1995).
Google Scholar 

76.
Fargues, J., Goettel, M. S., Smits, N., Ouedraogo, A. & Rougier, M. Effect of temperature on vegetative growth of Beauveria bassiana from different origins. Mycologia 89(3), 383–392 (1997).
Google Scholar 

77.
Ouedraogo, A., Fargues, J., Goettel, M. S. & Lomer, C. J. Effect of temperature on vegetative growth among isolates of Metarhizium anisopliae and M. flavoviride. Mycopathologia 137, 37–43 (1997).
CAS  PubMed  Google Scholar 

78.
Reyes, I. C., Bustillo, A. E. & Chaves, B. Efecto de Beauveria bassiana y Metarhizium anisopliae sobre el parasitoide de la broca del café, Cephalonomia stephanoderis. Rev. Colomb. Entomol. 21(4), 199–204 (1995).
Google Scholar 

79.
Castillo, A., Gómez, J., Infante, F. & Vega, F. E. Susceptibilidad del parasitoide Phymastichus coffea LaSalle (Hymenoptera: Eulophidae) a Beauveria bassiana en condiciones de laboratorio. Neotrop. Entomol. 38, 665–670 (2009).
PubMed  Google Scholar 

80.
Banu, J.G. Efficacy of entomopathogenic nematodes against coleopteran pests. In Biocontrol Agents: Entomopathogenic and Slug Parasitic Nematodes (eds Mahfouz, M.M. et al.) 174–192 (CABI, Oxfordshire, 2017).

81.
Aristizábal, L. F., Salazar, E. H. & Mejía, M. C. Cambios en la adopción de los componentes del manejo integrado de la broca del café Hypothenemus hampei (Coleoptera: Scolytidae) a través de metodologías participativas. Rev. Colomb. Entomol. 28(2), 153–160 (2002).
Google Scholar 

82.
O’Hara, R. B. & Kotze, D. J. Do not log-transform count data. Methods Ecol. Evol. 1, 118–122 (2010).
Google Scholar 

83.
Akaike, H. Information theory and an extension of the maximum likelihood principle. In Second International Symposium on Information Theory (eds. Petrov, V.N. & Csaki, F.) 267–281 (Academiai Kiado, Budapest, 1973).

84.
Georgescu-Roegen N. Energy and economic myths: institutional and analytical economic essays. Pergamon, New York, 1976) https://www.elsevier.com/books/energy-and-economic-myths/georgescu-roegen/978-0-08-021027-8.

85.
Neuenschwander, P. et al. Impact assessment of the biological control of the cassava mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae), by the introduced parasitoid Epidinocarsis lopezi (De Santis) (Hymenoptera: Encyrtidae). Bull. Entomol. Res. 79, 579–594 (1989).
Google Scholar 

86.
Gutierrez, A. P., Pitcairn, M. J., Ellis, C. K., Carruthers, N. & Ghezelbash, R. Evaluating biological control of yellow starthistle (Centaurea solstitialis) in California: a GIS based supply–demand demographic model. Biol. Control 34, 115–131 (2005).
Google Scholar 

87.
Gutierrez, A. P. & Ponti, L. Deconstructing the control of the spotted alfalfa aphid Therioaphis maculata. Agric. For. Entomol. 15, 272–284 (2013).
Google Scholar 

88.
Aristizábal, L. F. et al. Establishment of exotic parasitoids of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae) in Colombia through farmer participatory research. Int. J. Trop. Insect Sci. 32, 24–31 (2012).
Google Scholar 

89.
Vergara, J. D., Bustillo, A. E. & Cháves, B. Biología de Phymastichus coffea en condiciones de campo. Revista Cenicafé (Colombia) 52, 97–103 (2001).
Google Scholar 

90.
Johnson, M. A., Fortna, S., Hollingsworth, R. G. & Manoukis, N. C. Postharvest population reservoirs of coffee berry borer (Coleoptera: Curculionidae) on Hawai’i Island. J. Econ. Entomol. 112, 2833–2841 (2019).
PubMed  Google Scholar 

91.
Duque, H. & Cháves, C.B. Estudio Sobre la Adopción de Tecnología en Manejo Integrado de la Broca del café. Centro Nacional de Investigaciones del Café-Cenicafé, Chinchiná. https://books.google.com.co/books/about/Estudio_sobre_adopcion_del_manejo_integr.html?id=pDpGMwEACAAJ&redir_esc=y (2000).

92.
Bustillo, A. E. et al. Manejo integrado de la broca del café Hypothenemus hampei (Ferrari) en Colombia. Chinchiná, Colombia. Cenicafé, https://biblioteca.cenicafe.org/handle/10778/848 (1998).

93.
Aristizábal, L. F., Vélez, J. C. & León, C. A. Diagnóstico del manejo integrado de la broca del café, Hypothenemus hampei (Coleoptera: Curculionidae) con caficultores caldenses. Rev. Col. Entomol. 32, 117–124 (2006).
Google Scholar 

94.
Atallah, S. S., Gómez, M. I. & Jaramillo, J. A bioeconomic model of ecosystem services provision: Coffee Berry Borer and shade-grown coffee in Colombia. Ecol. Econ. 144, 129–138 (2018).
Google Scholar 

95.
Hernandez-Aguilera, J. N., Conrad, J. M., Gómez, M. I. & Rodewald, A. D. The economics and ecology of shade-grown coffee: A model to incentivize shade and bird conservation. Ecol. Econ. 159, 110–121 (2019).
Google Scholar 

96.
Infante, F. Pest management strategies against the coffee berry borer (Coleoptera:Curculionidae: Scolytinae). J. Agric. Food Chem. 66, 5275–5280 (2018).
CAS  PubMed  Google Scholar 

97.
Mendesil, E. et al. Semiochemicals used in host location by the coffee berryborer, Hypothenemus hampei. J. Chem. Ecol. 35(8), 944–950 (2009).
CAS  PubMed  Google Scholar 

98.
Borsa, P. & Gingerich, D. P. Allozyme variation and an estimate of the inbreeding coefficient in the coffee berry borer, Hypothenemus hampei (Coleoptera:Scolytidae). Bull. Entomol. Res. 85(1), 21–28 (1995).
CAS  Google Scholar 

99.
Gingerich, P. D., Borsa, P., Suckling, D. M. & Brun, L. O. Inbreeding in the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae) estimated from endosulfan resistance phenotype frequencies. Bull. Entomol. Res. 86, 667–674 (1996).
Google Scholar 

100.
Andreev, D., Breilid, H., Kirkendall, L., Brun, L. O. & Ffrench-Constant, R. H. Lack of nucleotide variability in a beetle pest with extreme inbreeding. Insect. Mol. Biol. 7(2), 197–200 (1998).
CAS  PubMed  Google Scholar 

101.
Benavides, P., Aspectos genéticos de la broca del Café. In La broca del café en América Tropical: Hallazgos y Enfoques. (eds Barrera J. F. et al.) 101–110 (Sociedad Mexicana de Entomología and El Colegio de la Frontera Sur, México, 2007). More

1.
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis. (Academic Press, New York, 2010).
2.
Campos-Soriano, L. & Segundo, B. S. New insights into the signaling pathways controlling defense gene expression in rice roots during the arbuscular mycorrhizal symbiosis. Plant Signal. Behav. 6, 553–557 (2011).
CAS  PubMed  PubMed Central  Google Scholar 

3.
He, X. H., Duan, Y. H., Chen, Y. L. & Xu, M. G. A 60-year journey of mycorrhizal research in China: Past, present and future directions. Sci. Chin. Life Sci. 53, 1374–1398 (2010).
Google Scholar 

4.
Mao, L. & Liu, Y. J. The eco-physiological functions of arbuscular mycorrhizal fungi: A review. Sciencepap. Online 11, 236–245 (2018).
Google Scholar 

5.
Karasawa, T., Hodge, A. & Fitter, A. H. Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant Cell Environ. 35, 819–828 (2012).
CAS  PubMed  Google Scholar 

6.
Pozo, M. J. & Azcón-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393–398 (2007).
CAS  PubMed  PubMed Central  Google Scholar 

7.
Parniske, M. Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775 (2008).
CAS  PubMed  Google Scholar 

8.
Bryla, D. R. & Eissenstat, D. M. Respiratory Costs of Mycorrhizal Associations. (eds. Lambers, H. & Ribas-Carbo, M.) 207–224 (Springer The Netherlands, 2005).

9.
Bonfante, P. & Genre, A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 48, 1038–1046 (2010).
Google Scholar 

10.
Rouphael, Y. et al. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci. Hortic. 196, 91–108 (2015).
Google Scholar 

11.
Veresoglou, S. D., Chen, B. D. & Rillig, M. C. Arbuscular mycorrhiza and soil nitrogen cycling. Soil Biol. Biochem. 46, 53–62 (2012).
CAS  Google Scholar 

12.
Galloway, J. N. et al. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
ADS  CAS  PubMed  PubMed Central  Google Scholar 

13.
Song, X. Z., Gu, H. H., Wang, M., Zhou, G. M. & Li, Q. Management practices regulate the response of Moso bamboo foliar stoichiometry to nitrogen deposition. Sci. Rep. 6, 24107 (2016).
ADS  CAS  PubMed  PubMed Central  Google Scholar 

14.
Galloway, J. N. & Cowling, E. B. Reactive nitrogen and the world: 200 years of change. Ambio 31, 64–71 (2002).
PubMed  Google Scholar 

15.
Liu, J. et al. Enhanced nitrogen deposition over China. Nature 494, 459–462 (2013).
ADS  CAS  PubMed  Google Scholar 

16.
Li, Q. et al. Nitrogen depositions increase soil respiration and decrease temperature sensitivity in a Moso bamboo forest. Agric. For. Meteorol. 268, 48–54 (2019).
ADS  Google Scholar 

17.
Wang, J. F. & Liu, N. K. Research progress on mechanisms of atmospheric nitrogen deposition and its ecological impact. Pollut. Control Technol. 31, 17–21+39 (2018).

18.
Lin, J. X. et al. Research progress on effects of nitrogen deposition on symbiont of plant-arbuscular mycorrhizal. Grassl. Turf 35, 88–94 (2015).
Google Scholar 

19.
Wang, Y. N. Physiological responses of Leymus chinens-arbuscular mycorrhizal symbiont to the interaction of nitrogen deposition and salt-alkali stress. PhD Thesis, Northeast Forestry University (2016).

20.
He, X. L., Liu, T. & Zhao, L. L. Effects of inoculating AM fungi on physiological characters and nutritional components of Astragalus membranaceus under different N application levels. Chin. J. Appl. Ecol. 20, 2118–2122 (2009).
CAS  Google Scholar 

21.
Hodge, A. The plastic plant, root responses to heterogeneous supplies of nutrients. New. Phytol. 162, 9–24 (2004).
Google Scholar 

22.
Lin, S. S. et al. Mycorrhizal studies and their application prospects in China. Acta Pratacult. Sin. 22, 310–325 (2013).
Google Scholar 

23.
Liu, R. J. & Chen, Y. L. Mycorrhizology. (Science Press, 2007).

24.
Su, Y. B., Lin, C., Zhang, F. S. & Yang, X. L. Effect of arbuscular mycorrhizal fungi (Glomus Mosseae, Glomus Versiformea, Gigaspora Margarita and Gigaspora Rosea) on phosphate activities and soil organic phosphate content in clover rhizosphere. Soils 35, 334–338 (2003).
CAS  Google Scholar 

25.
Feng, H. Y., Feng, G., Wang, J. G. & Li, X. L. Regulation of P status host plant on alkaline phosphatase (ALP) activity in intraradical hyphae and development of extraradical hyphae of AM fungi. Mycosystema 22, 589–598 (2003).
CAS  Google Scholar 

26.
Zhang, S. B., Wang, Y. S., Yin, X. F., Liu, J. B. & Wu, F. X. Development of arbuscular mycorrhizal (AM) fungi and their influences on the absorption of N and P of maize at different soil phosphorus application levels. J. Plant Nutr. Fertil. 23, 649–657 (2017).
Google Scholar 

27.
Shi, S. Z. et al. Ecophysiological effects of simulated nitrogen deposition on fine roots of Chinese fir (Cunninghamia lanceolata) seedlings. Acta Ecol. Sin. 37, 74–83 (2017).
Google Scholar 

28.
Slezack, S., Dumas-Gaudot, E., Paynot, M. & Gianinazzi, S. Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches?. Mol. Plant-Microbe Interact. 13, 238–241 (2000).
CAS  PubMed  Google Scholar 

29.
Yang, J. Y., Wang, Y. H., Wen, G. S. & Yi, L. T. Effects of AM fungi and simulated nitrogen deposition on the growth and biomass accumulation of Solidago canadensis seedlings. Chin. J. Ecol. 32, 2953–2958 (2013).
Google Scholar 

30.
Marschner, H. Marschner’s Mineral Nutrition of Higher Plants. (Academic Press, New York, 2012).

31.
García, I. V. & Mendoza, R. E. Relationships among soil properties, plant nutrition and arbuscular mycorrhizal fungi-plant symbioses in a temperate grassland along hydrologic, saline and sodic gradients. FEMS Microbiol. Ecol. 63, 359–371 (2008).
PubMed  Google Scholar 

32.
Johnson, N. C. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 185, 631–647 (2010).
CAS  PubMed  Google Scholar 

33.
Fitter, A. H. Costs and benefifits of mycorrhizas: implications for functioning under natural conditions. Experientia 47, 350–355 (1991).
Google Scholar 

34.
Pang, L., Zhou, Z. C., Zhang, Y. & Feng, Z. P. Effects of atmospheric N sedimentation on growth and P efficiency of Pinus Massoniana mycorrhizal seedlings under low P stress. J. Plant Nutr. Fertil. 22, 225–235 (2016).
CAS  Google Scholar 

35.
Johnson, N. C., Rowland, D. L., Corkidi, L., Egerton-Warburton, L. & Allen, E. B. Nitrogen enrichment alters mycorrhizal allocation at five mesic to semiarid grasslands. Ecology 84, 1895–1908 (2003).
Google Scholar 

36.
Cai, X. Z. Effects of nitrogen addition on arbuscular mycorrhizal fungi and nitrogen uptake of Chinese fir seedlings. PhD Thesis, Fujian Normal University (2017).

37.
Bago, B. et al. Differential morphogenesis of the extraradical mycelium of an arbuscular mycorrhizal fungus grown monoxenically on spatially heterogeneous culture media. Mycologia 96, 452–462 (2004).
PubMed  Google Scholar 

38.
Zhang, X. et al. Correlation between physicochemical properties of rhizosphere soil and arbuscular mycorrhizal fungi in Medicago sativa grassland. Northern Hortic. 13, 172–177 (2016).
Google Scholar 

39.
Wang, J. Effects of AM fungi on plant growth and community structure under different soil nitrogen fertility. PhD Thesis, Lanzhou University (2018).

40.
Holguin, G., Vazquez, P. & Bashan, Y. The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: An overview. Biol. Fertil. Soils. 33, 265–278 (2001).
CAS  Google Scholar 

41.
Ma, L. M., Wang, P. T. & Wang, S. G. Effect of flooding time length on mycorrhizal colonization of three AM fungi in two wetland plants. Environ. Sci. 35, 263–270 (2014).
Google Scholar 

42.
Sharma, D. & David, K. Moisture-a regulator of arbuscular mycorrhizal fungal community assembly and symbiotic phosphorus uptake. Mycorrhiza 25, 67–75 (2015).
Google Scholar 

43.
Zhang, X. H. The adaptability of arbuscular mycorrhizal fungi to different soil environmental factors. PhD Thesis, Agricultural University of Hebei (2003).

44.
Li, Y. F., Ju, L. H., Zhang, L. Y. & Xu, G. H. Effects of AM fungi on plant growth and nitrogen and phosphorus utilization in rice/mungbean intercropping under different phosphorus application levels. Jiangsu Agric. Sci. 41, 51–55 (2013).
CAS  Google Scholar 

45.
Kiers, E. T. et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880–882 (2011).
ADS  CAS  PubMed  Google Scholar 

46.
Read, D. J. Mycorrhizas in Ecosystems-Nature’s Response to the “Law of the Minimum”. (ed. Hawksworth, D.L.) 101–130 (CAB International, 1991).

47.
Sun, X. W. et al. Effects of eco-enviromental factors on the production and distribution of arbuscular mycorrhizal fungal spores. Acta Pratacult. Sin. 20, 214–221 (2011).
Google Scholar 

48.
Sun, J. H., Bi, Y. L., Qiu, L. & Jiang, B. A review about the effect of AMF on uptaking phosphorus by host plants in soil. Chin. J. Soil Sci. 47, 499–504 (2016).
Google Scholar 

49.
Subhashini, D. V. Effect of NPK fertilizers and co-inoculation with phosphate solubilising arbuscular mycorrhizal fungus and potassium mobilizing bacteria on growth, yield, nutrient acquisition and quality of tobacco (Nicotiana tabacum). Commun. Soil Sci. Plant Anal. 47, 328–337 (2016).
CAS  Google Scholar 

50.
Johnson, N. C., Wilson, G. W. T., Wilson, J. A., Miller, R. M. & Bowker, M. A. Mycorrhizal phenotypes and the law of the minimum. New Phytol. 205, 1473–1484 (2015).
CAS  PubMed  Google Scholar 

51.
Tessa, C. et al. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob. Change Biol. 20, 3646–3659 (2014).
Google Scholar 

52.
Gusewell, S. N: P ratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243–266 (2004).
Google Scholar 

53.
Xia, T. T., Wang, Z. P., Zhang, L. C. & Jing, H. R. Effects of phosphorus concentration on growth of arbuscular mycorrhizal sweet corn. Ind. Microbiol. 47, 49–53 (2017).
Google Scholar 

54.
Qiu, J. J. Molecular mechanism of phosphorus uptake by the interaction of arbuscular mycorrhizal fungi and maize. PhD Thesis, Shandong Agricultural University (2017).

55.
Reay, D. S., Dentener, F., Smith, P., Grace, J. & Feely, R. A. Global nitrogen deposition and carbon sinks. Nat. Geosci. 1, 430–437 (2008).
ADS  CAS  Google Scholar 

56.
Fang, H., Mo, J., Peng, S., Li, Z. & Wang, H. Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China. Plant Soil 297, 233–242 (2007).
CAS  Google Scholar 

57.
Mo, J. et al. Response of nutrient dynamics of decomposing pine (Pinus massoniana) needles to simulated N deposition in a disturbed and a rehabilitated forest in tropical China. Ecol. Res. 22, 649–658 (2007).
ADS  CAS  Google Scholar 

58.
Chen, Z. Y. et al. Relationship between growth and endogenous hormones of Chinese fir seedlings under low phosphorus stress. Sci. Silvae Sin. 52, 57–66 (2016).
Google Scholar 

59.
Leng, H. N. et al. Effects of phosphorous stress on the growth and nitrogen and phosphorus absorption of different formosan sweet gum provenances. Chin. J. Appl. Ecol. 20, 754–760 (2009).
CAS  Google Scholar 

60.
Wu, J. J. et al. Analysis of soil respiration and components in Castanopsis carlesii and Cunninghamia lanceolata plantations. Chin. J. Plant Ecol. 38, 45–53 (2014).
Google Scholar 

61.
Yang, Y. R. et al. Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol. Biochem. 86, 146–158 (2015).
CAS  Google Scholar 

62.
Berch, S. M. & Kendrick, B. Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74, 769–769 (1982).
Google Scholar 

63.
McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L. & Swan, J. A. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol. 115, 495–501 (1990).
Google Scholar 

64.
Gerdemann, J. W. & Nicolson, T. H. Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc. 46, 235–244 (1963).
Google Scholar 

65.
Eom, A. H., Wilson, G. W. & Hartnett, D. C. Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia 93, 233–242 (2001).
Google Scholar 

66.
Jackson, M. L. Soil chemical analysis. Soil Sci. 85, 288 (1973).
Google Scholar 

67.
Olsen, S. R. Estimation of available phosphorus in soils by extraction with sodium bicarbonate (U.S. Government Printing Office, New York, 1954).
Google Scholar 

68.
Hess, T. M. Tropical Soil Biology and Fertility: A Handbook of Methods. (eds Anderson, J. M. & Ingram, J. S. I.) 245–245 (CAB International, 1990).

69.
Zhang, W. R., Yang, G. J., Tu, X. N. & Zhang, P. Forestry Industry Standard of the People’s Republic of China: Forest Soil Analysis Method. (China Standards Press, 1999). More