Philippa Kaur

BirdLife International. Red List Update: Parrots of the Americas in Peril. https://www.birdlife.org/news/2021/02/08/red-list-update-parrots-of-the-americas-in-peril/ (2020).Berkunsky, I. et al. Current threats faced by Neotropical parrot populations. Biol. Cons. 214, 278–287. https://doi.org/10.1016/j.biocon.2017.08.016 (2017).Article 

Google Scholar 
ICMBIO—Instituto Chico Mendes de Conservação da Biodiversidade (Org.). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume III-Aves 709. https://www.icmbio.gov.br/portal/images/stories/comunicacao/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol3.pdf (Ministério do Meio Ambiente, 2018).CBRO—Comitê Brasileiro de Registros Ornitológicos. Listas das Aves do Brasil. 11th ed. http://www.cbro.org.br/wp-content/uploads/2020/06/avesbrasil_2014jan1.pdf (CBRO, 2014).Pacheco, J. F. et al. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee—second edition. Ornithol. Res. 29(2), 94–105. https://doi.org/10.1007/s43388-021-00058-x (2021).Article 

Google Scholar 
IUCN—International Union for Conservation of Nature. The IUCN Red List of Threatened Species www.iucnredlist.org (2018).Guedes, N. M. R. Biologia reprodutiva da arara azul (Anodorhynchus hyacinthinus) no Pantanal—MS, Brasil. (Dissertação de Mestrado Universidade de São Paulo, São Paulo (1993).Guedes, N. M. R. et al. Technical Report Assessing the Impact of Fire on Blue Macaws, Pantanal, Mato Grosso do Sul, Brazil, p 13, Campo Grande, Instituto Arara Azul (2019).Guedes, N. M. R. Araras azuis: 15 anos de estudos no Pantanal. In Paper presented at IV Simpósio Sobre Recursos Naturais e Sócio-Econômicos do Pantanal, Corumbá: Embrapa Pantanal (2004).Guedes, N. M. R. Sucesso reprodutivo, mortalidade e crescimento de filhotes de araras azuis Anodorhynchus hyacinthinus (Aves, Psittacidae), no Pantanal, Brasil (Tese de doutorado Universidade Estadual Paulista, Botucatu, 2009)Guedes, N. M. R. & Harper, L. H. Hyacinth macaws in the Pantanal. In The Large Macaws (eds Abramson, J. et al.) 394–421 (Raintree Publications, 1995).
Google Scholar 
Vicente, E. C. & Guedes, N. M. Organophosphate poisoning of Hyacinth Macaws in the Southern Pantanal, Brazil. Sci. Rep. 11, 1–6. https://doi.org/10.1038/s41598-021-84228-3 (2021).CAS 
Article 

Google Scholar 
Guedes, N. M. R. et al. Assessment of fire impact on Hyacinth Macaws in Perigara, Pantanal—MT, Brazil, p 35, Campo Grande, Instituto Arara Azul (2020).Guedes, N. M. R. et al. Macaws survive fires and provide hope for resilience—Stubborn survivors. Pantanal Sci. Mag. 6, 36–41 (2021).
Google Scholar 
Oliveira, M. D. R. et al. Lack of protected areas and future habitat loss threaten the Hyacinth Macaw Anodorhynchus hyacinthinus and its main food and nesting resources. Ibis 163, 1217–1234 (2021).Article 

Google Scholar 
Ricklefs, R. E. Patterns of growth in birds. Ibis 110, 419–451. https://doi.org/10.1111/j.1474-919X.1968.tb00058.x (1968).Article 

Google Scholar 
Gebhardt-Henrich, S. & Richner, H. Causes of growth variation and its consequences for fitness. Oxford Ornithol. Ser. 8, 324–339 (1998).
Google Scholar 
Masello, J. F. & Quillfeldt, P. Body size, body condition and ornamental feathers of Burrowing Parrots: Variation between years and sexes, assortative mating and influences on breeding success. Emu Austral Ornithol. 103, 149–161. https://doi.org/10.1071/MU02036 (2003).Article 

Google Scholar 
Renton, K. Influence of environmental variability on the growth of Lilac-crowned Parrot nestlings. Ibis 144, 331–339. https://doi.org/10.1046/j.1474-919X.2002.00015.x (2002).Article 

Google Scholar 
Masello, J. F. & Quillfeldt, P. Chick growth and breeding success of the Burrowing Parrot. Condor 104, 574–586. https://doi.org/10.1650/0010-5422 (2002).Article 

Google Scholar 
Pacheco, M. A., Beissinger, S. R. & Bosque, C. Why grow slowly in a dangerous place? Postnatal growth, thermoregulation, and energetics of nestling green-rumped parrotlets (Forpus passerinus). Auk 127, 558–570. https://doi.org/10.1525/auk.2009.09190 (2010).Article 

Google Scholar 
Vigo, G., Williams, M. & Brightsmith, D. J. Growth of Scarlet Macaw (Ara macao) chicks in southeastern Peru. Neotrop. Ornithol. 22, 143–153 (2011).
Google Scholar 
Lyon, J. P. et al. Reintroduction success of threatened Australian trout cod (Maccullochella macquariensis) based on growth and reproduction. Mar. Freshw. Res. 63, 598–605. https://doi.org/10.1071/MF12034 (2012).Article 

Google Scholar 
Vigo-Trauco, G., Garcia-Anleu, R. & Brightsmith, D. J. Increasing survival of wild macaw chicks using foster parents and supplemental feeding. Diversity 13, 121. https://doi.org/10.3390/d13030121 (2021).Article 

Google Scholar 
Tellería, J. L., De La Hera, I. & Perez-Tris, J. Morphological variation as a tool for monitoring bird populations: A review. Ardeola 60, 191–224. https://doi.org/10.13157/arla.60.2.2013.191 (2013).Article 

Google Scholar 
Silva, J. S. V. Elementos fisiográficos para delimitação do ecossistema Pantanal: Discussão e proposta. Oecol. Brasil. 1, 349–458. https://doi.org/10.4257/OECO.1995.0101.22 (1995).Article 

Google Scholar 
Silva, J. S. V. & Abdon, M. M. Delimitação do Pantanal Brasileiro e suas Sub-Regiões. Pesq. Agropec. Bras. 33, 1703–1711 (1998).
Google Scholar 
Keuroghlian, A., Eaton, D. & Desbiez, A. L. J. The response of a landscape species, white-lipped peccaries, to seasonal resource fluctuations in a tropical wetland, the Brazilian Pantanal. Int. J. Biodivers. Conserv. 1, 87–97 (2009).
Google Scholar 
Donatelli, R. J., Posso, S. R. & Toledo, M. C. B. D. Distribution, composition and seasonality of aquatic birds in the Nhecolândia sub-region of South Pantanal, Brazil. Braz. J. Biol. 74, 844–853 (2014).CAS 
Article 

Google Scholar 
Donatelli, R. J. et al. Temporal and spatial variation of richness and abundance of the community of birds in the Pantanal wetlands of Nhecolândia (Mato Grosso do Sul, Brazil). Rev. Biol. Trop. 65, 1358–1380 (2017).Article 

Google Scholar 
Tomas, W. M. et al. Sustainability agenda for the Pantanal Wetland: Perspectives on a collaborative interface for science, policy, and decision-making. Trop. Conserv. Sci. 12, 1–30. https://doi.org/10.1177/1940082919872634 (2019).ADS 
Article 

Google Scholar 
Harris, M. B. et al. Safeguarding the Pantanal wetlands: Threats and conservation initiatives. Conserv. Biol. 19, 714–720. https://doi.org/10.1111/j.1523-1739.2005.00708.x (2005).Article 

Google Scholar 
Santos Júnior, A. D., Aspectos populacionais de Sterculia apetala (Jacq.) Karst (Sterculiaceae) como subsídios ao plano de conservação da arara-azul no Sul do Pantanal, Mato Grosso do Sul, Brasil. (2006). https://repositorio.ufms.br/handle/123456789/521.Ricklefs, R. E. The optimization of growth rate in altricial birds. Ecology 65, 1602–1616 (1984).Article 

Google Scholar 
Bruford, M. W., Hanotte, O., Brookfield, J. F. Y. & Burke, T. Single-locus and multilocus DNA fingerprinting. In Molecular Genetic Analysis of Populations: A Practical Approach (ed. Hoelzel, A. R.) 225–269 (Oxford University Press, 1992).
Google Scholar 
Miyaki, C. Y. et al. Sex identification of parrots, toucans, and curassows by PCR: Perspectives for wild and captive population studies. Zoo Biol. 17(5), 415–423 (1998).Article 

Google Scholar 
Cavanaugh, J. E. & Neath, A. A. The Akaike information criterion: Background, derivation, properties, application, interpretation, and refinements. Wiley Interdiscip. Rev. Comput. Stat. 11, 1460. https://doi.org/10.1002/wics.1460 (2019).MathSciNet 
Article 

Google Scholar 
Motulsky H. J. GraphPad curve fitting guide. 2021. http://www.graphpad.com/guides/prism/7/curve-fitting/index.htm. Accessed 18 September.Saunders, D. A., Smith, G. T. & Rowley, I. The availability and dimensions of tree hollows that provide nest sites for cockatoos (Psittaciformes) in Western Australia. Wildl. Res. 9, 541–556. https://doi.org/10.1071/WR9820541 (1982).Article 

Google Scholar 
Navarro, J. L. & Bucher, E. H. Growth of monk parakeets. Wilson Bull. 102, 520–525 (1990).
Google Scholar 
Murtaugh, P. A. Performance of several variable-selection methods applied to real ecological data. Ecol. Lett. 12, 1061–1068 (2009).Article 

Google Scholar 
Waltman, J. R. & Beissinger, S. R. Breeding behavior of the Green-rumped Parrotlet. Wilson Bull. 104, 65–84 (1992).
Google Scholar 
Enkerlin-Hoeflich, E. C., Packard, J. M. & González-Elizondo, J. J. Safe field techniques for nest inspections and nestling crop sampling of parrots. J. Field Ornithol. 70, 8–17 (1999).
Google Scholar 
Barros, Y. de M. Biologia comportamental de Propyrrhura maracana (Aves, Psittacidae): Fundamentos para conservação in situ de Cyanopsitta spixii (Aves, Psittacidae) na Caatinga. (Tese de Doutorado Universidade Estadual de São Paulo, Rio Claro, 2001).Seixas, G. H. F. & Mourão, G. M. Growth of nestlings of the BlueFronted Amazon (Amazona aestiva) raised in the wild or in captivity. Ornitol. Neotrop. 14, 295–305 (2003).
Google Scholar 
Vigo-Trauco, G. Crecimiento de pichones de Guacamayo Escarlata, Ara macao (Linneus: 1758) en la Reserva Nacional Tambopata-Madre de Dios-Peru (Tese Universidad Nacional Agraria La Molina, 2007).
Google Scholar 
Tjørve, K. M. & Tjørve, E. The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family. PLoS One https://doi.org/10.1371/journal.pone.0178691 (2017).Article 
PubMed 
PubMed Central 
MATH 

Google Scholar 
Reed, J. M. The role of behavior in recent avian extinctions and endangerments. Conserv. Biol. 13, 232–241. https://doi.org/10.1046/j.1523-1739.1999.013002232.x (1999).Article 

Google Scholar 
Tjørve, K. M., Underhill, L. G. & Visser, G. H. Energetics of growth in semi-precocial shorebird chicks in a warm environment: The African black oystercatcher, Haematopus moquini. Zoology 110, 176–188. https://doi.org/10.1016/j.zool.2007.01.002 (2007).Article 
PubMed 

Google Scholar 
Tjørve, K. M., Underhill, L. G. & Visser, G. H. The energetic implications of precocial development for three shorebird species breeding in a warm environment. Ibis 150, 125–138 (2008).Article 

Google Scholar 
Ricklefs, R. E. Weight recession in nestling birds. Auk 85, 30–35. https://doi.org/10.2307/4083621 (1968).Article 

Google Scholar 
Huin, N. & Prince, P. A. Chick growth in albatrosses: Curve fitting with a twist. J. Avian Biol. 31, 418–425. https://doi.org/10.1034/j.1600-048X.2000.310318.x (2000).Article 

Google Scholar 
Corsini, M. et al. Growing in the city: Urban evolutionary ecology of avian growth rates. Evol. Appl. 14, 69–84. https://doi.org/10.1111/eva.13081 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Barbosa, L. T. Avaliação do sucesso reprodutivo da arara-canindé (Ara ararauna—Psittacidae) e o desenvolvimento urbano de Campo Grande, Mato Grosso do Sul (Dissertação de mestrado Universidade Anhanguera Uniderp, Campo Grande, 2015).Giraldo-Deck, L. M. et al. Development of intraspecific size variation in black coucals, white-browed coucals and ruffs from hatching to fledging. J. Avian Biol. 51, e02440. https://doi.org/10.1111/jav.02440 (2020).Article 

Google Scholar 
Guedes et al. Annual Technical Report from the Instituto Arara Azul., Pantanal-MS, Brazil. 35p, Campo Grande, Instituto Arara Azul (2022). More

Yu, Z., Loisel, J., Brosseau, D. P., Beilman, D. W. & Hunt, S. J. Global peatland dynamics since the Last Glacial Maximum. Geophys. Res. Lett. 37, 13 (2010).
Google Scholar 
Leifeld, J., Wüst-Galley, C. & Page, S. Intact and managed peatland soils as a source and sink of GHGs from 1850 to 2100. Nat. Clim. Change 9, 945–947 (2019).CAS 
Article 

Google Scholar 
Turetsky, M. R. et al. Carbon release through abrupt permafrost thaw. Nat. Geosci. 13, 138–143 (2020).CAS 
Article 

Google Scholar 
Evans, C. D. et al. Overriding water table control on managed peatland greenhouse gas emissions. Nature 593, 548–552 (2021).CAS 

Google Scholar 
Bonn, A. et al. Investing in nature: Developing ecosystem service markets for peatland restoration. Ecosyst. Serv. 9, 54–65 (2014).Article 

Google Scholar 
Martin-Ortega, J., Allott, T. E., Glenk, K. & Schaafsma, M. Valuing water quality improvements from peatland restoration: evidence and challenges. Ecosyst. Serv. 9, 34–43 (2014).Article 

Google Scholar 
Loisel, J. et al. Expert assessment of future vulnerability of the global peatland carbon sink. Nat. Clim. Change 11, 70–77 (2021).Article 

Google Scholar 
Chimner, R. A., Cooper, D. J., Wurster, F. C. & Rochefort, L. An overview of peatland restoration in North America: where are we after 25 years? Restor. Ecol. 25, 283–292 (2017).Article 

Google Scholar 
Andersen, R. et al. An overview of the progress and challenges of peatland restoration in Western Europe. Restor. Ecol. 25, 271–282 (2017).Article 

Google Scholar 
Bossio, D. A. et al. The role of soil carbon in natural climate solutions. Nat. Sustain. 3, 391–398 (2020).Article 

Google Scholar 
Humpenöder, F. et al. Peatland protection and restoration are key for climate change mitigation. Environ. Res. Lett. 15, 104093 (2020).Article 

Google Scholar 
Drever, C. R. et al. Natural climate solutions for Canada. Sci. Adv. 7, https://doi.org/10.1126/sciadv.abd6034 (2020).Leifeld, J. & Menichetti, L. The underappreciated potential of peatlands in global climate change mitigation strategies. Nat. Commun. 9, 1–7 (2018).CAS 
Article 

Google Scholar 
Gunderson, L. H. Ecological resilience—in theory and application. Annu. Rev. Ecol. Syst. 31, 425–439 (2000).Article 

Google Scholar 
Sasaki, T., Furukawa, T., Iwasaki, Y., Seto, M. & Mori, A. S. Perspectives for ecosystem management based on ecosystem resilience and ecological thresholds against multiple and stochastic disturbances. Ecol. Indic. 57, 395–408 (2015).Article 

Google Scholar 
Scheffer, M. Critical transitions in nature and society (Princeton University, 2009).Alexandrov, G. A., Brovkin, V. A., Kleinen, T. & Yu, Z. The capacity of northern peatlands for long-term carbon sequestration. Biogeosciences 17, 47–54 (2020).CAS 
Article 

Google Scholar 
Page, S. E. & Baird, A. J. Peatlands and global change: response and resilience. Annu. Rev. Environ. Resour. 41, 35–57 (2016).Article 

Google Scholar 
Rydin, H., Jeglum, J. K. & Bennett, K. D. The biology of peatlands, 2nd edition (Oxford University Press, 2013).Kim, J. et al. Water table fluctuation in peatlands facilitates fungal proliferation, impedes Sphagnum growth and accelerates decomposition. Front. Earth Sci. 8, 717 (2021).
Google Scholar 
IPCC. Climate Change 2022: Impacts, Adaptation, and Vulnerability (Cambridge University Press, In Press).Belyea, L. R. Non-linear dynamics of peatlands and potential feedbackson the climate system, in Northern Peatlands and Carbon Cycling (A, Baird. et al. eds), pp 5–18 (American Geophysical Union Monograph Series, 2009).Holden, J. et al. Overland flow velocity and roughness properties in peatlands. Water Resour. Res. 44, https://doi.org/10.1029/2007WR006052 (2008).Holden, J., Wallage, Z. E., Lane, S. N. & McDonald, A. T. Water table dynamics in undisturbed, drained and restored blanket peat. J. Hydrol. 402, 103–114 (2011).Article 

Google Scholar 
Glaser, P. H. et al. Surface deformations as indicators of deep ebullition fluxes in a large northern peatland. Glob. Biogeochem. Cycles 18, GB1003 (2004).Article 
CAS 

Google Scholar 
Belyea, L. R. & Baird, A. J. Beyond “the limits to peat bog growth”: cross‐scale feedback in peatland development. Ecol. Monogr. 76, 299–322 (2006).Article 

Google Scholar 
Waddington, J. M. et al. Hydrological feedbacks in northern peatlands. Ecohydrology 8, 113–127 (2015).Article 

Google Scholar 
Holden, J., Evans, M. G., Burt, T. P. & Horton, M. Impact of land drainage on peatland hydrology. J. Environ. Qual. 35, 1764–1778 (2006).CAS 
Article 

Google Scholar 
Liu, H. & Lennartz, B. Hydraulic properties of peat soils along a bulk density gradient—a meta study. Hydrol. Process. 33, 101–114 (2019).Article 

Google Scholar 
Gałka, M., Tobolski, K., Górska, A. & Lamentowicz, M. Resilience of plant and testate amoeba communities after climatic and anthropogenic disturbances in a Baltic bog in Northern Poland: implications for ecological restoration. Holocene 27, 130–141 (2017).Article 

Google Scholar 
Lamentowicz, M. et al. Unveiling tipping points in long-term ecological records from Sphagnum-dominated peatlands. Biol. Lett. 15, https://doi.org/10.1098/rsbl.2019.0043 (2019).van der Velde, Y. Emerging forest-peatland bistability and resilience of European peatland carbon stores. Proc. Natl Acad. Sci. 118, https://doi.org/10.1073/pnas.210174211 (2021).Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).CAS 
Article 

Google Scholar 
Minayeva, T. Y. & Sirin, A. A. Peatland biodiversity and climate change. Biol. Bull. Rev. 2, 164–175 (2012).Article 

Google Scholar 
Minayeva, T. Y., Bragg, O. & Sirin, A. A. Towards ecosystem-based restoration of peatland biodiversity. Mires Peat 19, 1–36 (2017).
Google Scholar 
Andersen, R., Chapman, S. J. & Artz, R. R. Microbial communities in natural and disturbed peatlands: a review. Soil Biol. Biochem. 1, 979–994 (2013).Article 
CAS 

Google Scholar 
van Breemen, N. How Sphagnum bogs down other plants. Trends Ecol. Evol. 10, 270–275 (1995).Article 

Google Scholar 
Hugron, S. & Rochefort, L. Sphagnum mosses cultivated in outdoor nurseries yield efficient plant material for peatland restoration. Mires Peat 20, 1–6 (2018).
Google Scholar 
Vitt, D. H. Peatlands: ecosystems dominated by bryophytes. In: Shaw A. J. & Goffinet B. (eds) Bryophyte biology, pp 312–343 (Cambridge University Press, 2002).Yu, Z. et al. Carbon sequestration in western Canadian peat highly sensitive to Holocene wet-dry climate cycles at millennial timescales. Holocene 13, 801–808 (2003).Article 

Google Scholar 
Chiapusio, G. et al. Sphagnum species module their phenolic profiles and mycorrhizal colonization of surrounding Andromeda polifolia along peatland microhabitats. J. Chem. Ecol. 44, 1146–1157 (2018).CAS 
Article 

Google Scholar 
Sherwood, J. H. et al. Effect of drainage and wildfire on peat hydrophysical properties. Hydrol. Process. 27, 1866–1874 (2013).Article 

Google Scholar 
Tanneberger, F., Flade, M., Preiksa, Z. & Schröder, B. Habitat selection of the globally threatened aquatic warbler Acrocephalus paludicola at the western margin of its breeding range and implications for management. Ibis 152, 347–358 (2010).Article 

Google Scholar 
Kreyling, J. Rewetting does not return drained fen peatlands to their old selves. Nat. Commun. 12, 1–8 (2021).Article 
CAS 

Google Scholar 
Ritson, J. P. et al. Towards a microbial process-based understanding of the resilience of peatland ecosystem service provisioning–a research agenda. Sci. Total Environ. 759, https://doi.org/10.1016/j.scitotenv.2020.143467 (2021).Secco, E. D., Haapalehto, T., Haimi, J., Meissner, K. & Tahvanainen, T. Do testate amoebae communities recover in concordance with vegetation after restoration of drained peatlands? Mires Peat 18, https://doi.org/10.19189/MaP.2016.OMB.231 (2016).Basiliko, N. et al. Controls on bacterial and archaeal community structure and greenhouse gas production in natural, mined, and restored Canadian peatlands. Front. Microbiol. 31, https://doi.org/10.3389/fmicb.2013.00215 (2013).Barber, K. E. Peat stratigraphy and climatic change. vol 219, (AA Balkema, 1981).Quinton, W. L. & Roulet, N. T. Spring and summer runoff hydrology of a subarctic patterned wetland. Arctic Alpine Res. 30, 285–294 (1998).Article 

Google Scholar 
Eppinga, M. B., Rietkerk, M., Wassen, M. J. & De Ruiter, P. C. Linking habitat modification to catastrophic shifts and vegetation patterns in bogs. Plant Ecol. 200, 53–68 (2009).Article 

Google Scholar 
Bragazza, L., Parisod, J., Buttler, A. & Bardgett, R. D. Biogeochemical plant– soil microbe feedback in response to climate warming in peatlands. Nat. Clim. Change 3, 273–277 (2013).CAS 
Article 

Google Scholar 
Fenton, N. J. Applied ecology in Canada’s boreal: a holistic view of the mitigation hierarchy and resilience theory. Botany 94, 1009–1014 (2016).Article 

Google Scholar 
Xu, L. X. et al. Maintain spatial heterogeneity, maintain biodiversity—a seed bank study in a grazed alpine fen meadow. Land Degrad. Dev. 28, 1376–1385 (2017).Article 

Google Scholar 
Laine, J., Vasander, H. & Laiho, R. Long-term effects of water level drawdown on the vegetation of drained pine mires in southern Finland. J. Appl. Ecol. 1, 785–802 (1995).
Google Scholar 
Gatis, N. et al. The effect of drainage ditches on vegetation diversity and CO2 fluxes in a Molinia caerulea‐dominated peatland. Ecohydrology 9, 407–420 (2016).CAS 
Article 

Google Scholar 
Swindles, G. T. et al. Resilience of peatland ecosystem services over millennial timescales: evidence from a degraded British bog. Journal of Ecology 104, 621–636 (2016).Article 

Google Scholar 
Liu, H., Gao, C. & Wang, G. Understand the resilience and regime shift of the wetland ecosystem after human disturbances. Sci. Total Environ. 643, 1031–1040 (2018).CAS 
Article 

Google Scholar 
Couwenberg, J. et al. Assessing greenhouse gas emissions from peatlands using vegetation as a proxy. Hydrobiologia 674, 67–89 (2011).CAS 
Article 

Google Scholar 
Tiemeyer, B. et al. High emissions of greenhouse gases from grasslands on peat and other organic soils. Glob. Change Biol. 22, 4134–4149 (2016).Article 

Google Scholar 
Strack, M. et al. Controls on plot-scale growing season CO2 and CH4 fluxes in restored peatlands: do they differ from unrestored and natural sites? Mires Peat 17, 1–18 (2016).
Google Scholar 
Nugent, K. A., Strachan, I. B., Strack, M., Roulet, N. T. & Rochefort, L. Multi-year net ecosystem carbon balance of a restored peatland reveals a return to carbon sink. Global Change Biol. 24, 5751–5768 (2018).Article 

Google Scholar 
Hambley, G. et al. Net ecosystem exchange from two formerly afforested peatlands undergoing restoration in the Flow Country of northern Scotland. Mires Peat 23, https://doi.org/10.19189/MaP.2018.DW.346 (2019).Schwieger, S. et al. Wetter is better: rewetting of minerotrophic peatlands increases plant production and moves them towards carbon sinks in a dry year. Ecosystems 24, 1093–1109 (2021).CAS 
Article 

Google Scholar 
Poulin, M., Andersen, R. & Rochefort, L. A new approach for tracking vegetation change after restoration: a case study with peatlands. Restor. Ecol. 21, 363–371 (2013).Article 

Google Scholar 
Gonzalez, E. & Rochefort, L. Drivers of success in 53 cutover bogs restored by a moss layer transfer technique. Ecol. Eng. 68, 279–290 (2014).Article 

Google Scholar 
Karofeld, E., Müür, M. & Vellak, K. Factors affecting re-vegetation dynamics of experimentally restored extracted peatland in Estonia. Environ. Sci. Pollut. Res. 23, 13706–13717 (2016).Article 

Google Scholar 
Karofeld, E., Kaasik, A. & Vellak, K. Growth characteristics of three Sphagnum species in restored extracted peatland. Restor. Ecol. 28, 1574–1583 (2020).Article 

Google Scholar 
Purre, A. H., Ilomets, M., Truus, L., Pajula, R. & Sepp, K. The effect of different treatments of moss layer transfer technique on plant functional types biomass in revegetated milled peatlands. Restor. Ecol. 28, 1584–1595 (2020).Article 

Google Scholar 
Beyer, F. et al. Drought years in peatland rewetting: rapid vegetation succession can maintain the net CO2 sink function. Biogeosciences 18, 917–935 (2021).CAS 
Article 

Google Scholar 
Ketcheson, S. J. & Price, J. S. The impact of peatland restoration on the site hydrology of an abandoned block-cut bog. Wetlands 31, 1263–1274 (2011).Article 

Google Scholar 
McCarter, C. P. R. & Price, J. S. The hydrology of the Bois-des-Bel bog peatland restoration: 10 years post-restoration. Ecol. Eng. 55, 73–81 (2013).Article 

Google Scholar 
Koebsch, F. et al. The impact of occasional drought periods on vegetation spread and greenhouse gas exchange in rewetted fens. Philos. Transac. R. Soc. B 375, https://doi.org/10.1098/rstb.2019.0685 (2020).Blier‐Langdeau, A., Guêné‐Nanchen, M., Hugron, S. & Rochefort, L. The resistance and short‐term resilience of a restored extracted peatland ecosystems post‐fire: an opportunistic study after a wildfire. Restor. Ecol. 30, https://doi.org/10.1111/rec.13545 (2022).Rochefort, L., Quinty, F., Campeau, S., Johnson, K. & Malterer, T. North American approach to the restoration of Sphagnum dominated peatlands. Wetlands Ecol. Manage. 11, 3–20 (2003).CAS 
Article 

Google Scholar 
Lavoie, C., St-Louis, A. & Lachance, D. Vegetation dynamics on an abandoned vacuum-mined peatland: Five years of monitoring. Wetlands Ecol. Manage. 13, 621–633 (2005).Article 

Google Scholar 
Poulin, M., Rochefort, L., Quinty, F. & Lavoie, C. Spontaneous revegetation of mined peatlands in eastern Canada. Can. J. Botany 83, 539–557 (2005).Article 

Google Scholar 
Quinty, F., LeBlanc, M.-C. & Rochefort, L. Peatland Restoration Guide—PERG, CSPMA and APTHQ (Université Laval, 2020).Wagner, D. J. & Titus, J. E. Comparative desiccation tolerance of two Sphagnum mosses. Oecologia 62, 182–187 (1984).Article 

Google Scholar 
Gonzalez, E. & Rochefort, L. Declaring success in Sphagnum peatland restoration: identifying outcomes from readily measurable vegetation descriptors. Mires Peat 24, 1–16 (2019).
Google Scholar 
Scotland National Peatland Plan. Working for our future. https://www.nature.scot/doc/scotlands-national-peatland-plan-working-our-future#:~:text=The%202020%20Challenge%20for%20Scotland’s,more%20resilient%20to%20climate%20change (2020).Wilkie, N. M. & Mayhew, P. W. The management and restoration of damaged blanket bog in the north of Scotland. Bot. J. Scotl. 55, 125–133 (2003).Article 

Google Scholar 
Hancock, M. H., Klein, D., Andersen, R. & Cowie, N. R. Vegetation response to restoration management of a blanket bog damaged by drainage and afforestation. Appl. Veg. Sci. 21, 167–178 (2018).Article 

Google Scholar 
Harris, A. & Baird, A. J. Microtopographic drivers of vegetation patterning in blanket peatlands recovering from erosion. Ecosystems 22, 1035–1054 (2019).Article 

Google Scholar 
Bradley, A. V., Andersen, R., Marshall, C., Sowter, A. & Large, D. J. Identification of typical ecohydrological behaviours using InSAR allows landscape-scale mapping of peatland condition. Earth Surf. Dyn. 10, 261–277 (2022).Article 

Google Scholar 
Gaffney, P. P., Hancock, M. H., Taggart, M. A. & Andersen, R. Measuring restoration progress using pore-and surface-water chemistry across a chronosequence of formerly afforested blanket bogs. J. Environ. Manage. 219, 239–251 (2018).CAS 
Article 

Google Scholar 
Hermans, R. et al. Climate benefits of forest-to-bog restoration on deep peat–Policy briefing. Climate X Change 1–5, https://www.climatexchange.org.uk/media/3654/climate-benefits-of-forest-to-bog-restoration-on-deep-peat.pdf (2019).Wilson, D. et al. Greenhouse gas emission factors associated with rewetting of organic soils. Mires Peat 17, 1–28 (2016).
Google Scholar 
Günther, A. et al. Prompt rewetting of drained peatlands reduces climate warming despite methane emissions. Nat. Commun. 11, 1–5 (2020).Article 
CAS 

Google Scholar 
Young, D. M. et al. Misinterpreting carbon accumulation rates in records from near-surface peat. Sci. Rep. 9, 1–8 (2019).Article 
CAS 

Google Scholar 
Young, D. M., Baird, A. J., Gallego-Sala, A. V. & Loisel, J. A cautionary tale about using the apparent carbon accumulation rate (aCAR) obtained from peat cores. Sci. Rep. 11, 9547 (2021).CAS 
Article 

Google Scholar 
Klimkowska, A. et al. Are we restoring functional fens? The outcomes of restoration projects in fens re-analysed with plant functional traits. PLoS One 14, https://doi.org/10.1371/journal.pone.0215645 (2019).Huth, V. et al. The climate benefits of topsoil removal and Sphagnum introduction in raised bog restoration. Restor. Ecol. 30, https://doi.org/10.1111/rec.13490 (2022).Schimelpfenig, D., Cooper, D. J. & Chimner, R. A. Effectiveness of ditch blockage for restoring hydrologic and soil processes in mountain peatlands. Restor. Ecol. 22, 257–265 (2014).Article 

Google Scholar 
Laine, A. M., Tolvanen, A., Mehtätalo, L. & Tuittila, E. S. Vegetation structure and photosynthesis respond rapidly to restoration in young coastal fens. Ecol. Evol. 6, 6880–6891 (2016).Article 

Google Scholar 
Gallego-Sala, A. V. & Prentice, I. C. Blanket peat biome endangered by climate change. Nat. Clim. Change 3, 152–155 (2013).Article 

Google Scholar 
Schneider, R. R., Devito, K., Kettridge, N. & Bayne, E. Moving beyond bioclimatic envelope models:50 integrating upland forest and peatland processes to predict ecosystem transitions under climate change in the51 western Canadian boreal plain: Western boreal ecosystem transitions under climate change. Ecohydrology 9, 899–908 (2016).Article 

Google Scholar 
Blundell, A. & Holden, J. Using palaeoecology to support blanket peatland management. Ecol. Indic. 49, 110–120 (2005).Article 

Google Scholar 
Newman, S. et al. Drivers of landscape evolution: multiple regimes and their influence on carbon sequestration in a sub‐tropical peatland. Ecol. Monogr. 87, 578–599 (2017).Article 

Google Scholar 
Wilkinson, S. L., Moore, P. A., Flannigan, M. D., Wotton, B. M. & Waddington, J. M. Did enhanced afforestation cause high severity peat burn in the Fort McMurray Horse River wildfire? Environ. Res. Lett. 13, https://doi.org/10.1088/1748-9326/aaa136 (2018).Hokanson, K. J. et al. A hydrogeological landscape framework to identify peatland wildfire smouldering hot spots. Ecohydrology 11, https://doi.org/10.1002/eco.1942 (2018).IPCC. Global warming of 1.5 °C (IPCC, 2018).Glenk, K., Faccioli, M., Martin-Ortega, J., Schulze, C. & Potts, J. The opportunity cost of delaying climate action: Peatland restoration and resilience to climate change. Glob. Environ. Change 70, https://doi.org/10.1016/j.gloenvcha.2021.102323 (2021).Tanneberger, F. et al. The power of nature‐based solutions: how peatlands can help us to achieve key EU sustainability objectives. Adv. Sustain. Syst. 5, https://doi.org/10.1002/adsu.202000146 (2021).Loisel, J. & Walenta, J. Carbon parks could secure essential ecosystems for climate stabilization. Nat. Ecol. Evol. 6, 486–488 (2022).Article 

Google Scholar 
Morecroft, M. D. et al. Measuring the success of climate change adaptation and mitigation in terrestrial ecosystems. Science 366, eaaw9256 (2019).Terzano, D. Community‐led peatland restoration in Southeast Asia: 5Rs approach. Restor. Ecol. 3, https://doi.org/10.1111/rec.13642 (2022). More

Galloway, J. N., Townsend, W. H., Erisman, J. W., Bekunda, M. & Cai, Z. Transformation of the nitrogen cycle: Recent trends, questions and potential solutions. Science 320, 889–892 (2008).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Phoenix, G. K. et al. Impacts of atmospheric nitrogen deposition: Responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob. Change Biol. 18, 1197–1215 (2012).ADS 
Article 

Google Scholar 
Pons, T. L., van der, Werf, A. & Lambers, H. Photosynthetic nitrogen use efficiency of inherently slow- and fast-growing species: Possible explanations for observed differences. In A Whole Plant Perspective on Carbon-Nitrogen Interactions (eds Roy, J., Garnier, E.) 61–77 (SPB Academic Publishing, The Hague, 1994).Ai, Z. M., Xue, S., Wang, G. L. & Liu, G. B. Responses of Non-structural carbohydrates and C:N: P stoichiometry of Bothriochloa ischaemum to nitrogen addition on the Loess Plateau, China. J. Plant Growth Regul. 36, 714–722 (2017).CAS 
Article 

Google Scholar 
Marklein, A. R. & Houlton, B. Z. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol. 193, 696–704 (2012).CAS 
PubMed 
Article 

Google Scholar 
Dietze, M. C. et al. Nonstructural carbon in woody plants. Annu. Rev. Plant Biol. 65, 667–687 (2014).CAS 
PubMed 
Article 

Google Scholar 
Hartmann, H. & Trumbore, S. Understanding the roles of nonstructural carbohydrates in forest trees -from what we can measure to what we want to know. New Phytol. 211, 386–403 (2016).CAS 
PubMed 
Article 

Google Scholar 
Yang, Q. P. et al. Different responses of non-structural carbohydrates in above-ground tissues/organs and root to extreme drought and re-watering in Chinese fir (Cunninghamia lanceolata) saplings. Trees 30, 1863–1871 (2016).CAS 
Article 

Google Scholar 
Peng, Z. T. et al. Non-structural carbohydrates regulated by nitrogen and phosphorus fertilization varied with organs and fertilizer levels in Moringa oleifera Seedlings. J. Plant Growth Regul. 40, 1777–1786 (2021).CAS 
Article 

Google Scholar 
Nardini, A. et al. Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms deferentially affected by an extreme summer drought. Plant Cell Environ. 39, 618–627 (2016).CAS 
PubMed 
Article 

Google Scholar 
Wang, F. C. et al. Effects of experimental nitrogen addition on nutrients and nonstructural carbohydrates of dominant understory plants in a Chinese Fir plantation. Forests 10, 155 (2019).Article 

Google Scholar 
Elser, J. J. et al. Growth rate-stoichiometry couplings in diverse biota. Ecol. Lett. 6, 936–943 (2003).Article 

Google Scholar 
Jinm, X. M. et al. Ecological stoichiometry and biomass response of Agropyron michnoi under simulated N deposition in a sandy grassland, China. J. Arid Land. 12, 741–751 (2020).Article 

Google Scholar 
Jing, H. et al. Nitrogen addition changes the stoichiometry and growth rate of different organsin pinus tabuliformis seedlings. Front. Plant Sci. 8, 1922 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Zhan, S. X., Wang, Y., Zhu, Z. C., Li, W. H. & Bai, Y. F. Nitrogen enrichment alters plant N: P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem. Environ. Exp. Bot. 134, 21–32 (2017).CAS 
Article 

Google Scholar 
Stiling, P. & Cornelissen, T. How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2 -mediated changes on plant chemistry and herbivore performance. Glob. Change Biol. 13, 1823–1842 (2007).ADS 
Article 

Google Scholar 
Wang, X. G. et al. Responses of C:N: P stoichiometry of plants from a Hulunbuir grassland to salt stress, drought and nitrogen addition. Phyton-Int. J. Exp. Bot. 87, 123–132 (2018).
Google Scholar 
Liu, X. J. et al. Enhanced nitrogen deposition over China. Nature 494, 459–462 (2013).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Huang, W. J., Houlton, B. Z., Marklein, A. R., Liu, J. X. & Zhou, G. Y. Plant stoichiometric responses to elevated CO2 vary with nitrogen and phosphorus inputs: Evidence from a global-scale meta-analysis. Sci. Rep. 5, 18225 (2015).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Wang, X. et al. Effects of nutrient addition on nitrogen, phosphorus and non-structural carbohydrates concentrations in leaves of dominant plant species in a semiarid steppe. Chin. J. Ecol. 33, 1795–1802 (2014).
Google Scholar 
Yang, D. X., Song, L. & Jin, G. Z. The soil C:N: P stoichiometry is more sensitive than the leaf C:N: P stoichiometry to nitrogen addition: A four-year nitrogen addition experiment in a Pinus koraiensis plantation. Plant Soil 442, 183–198 (2019).CAS 
Article 

Google Scholar 
Chong, P. F., Zhan, J., Li, Y. & Jia, X. Y. Carbon dioxide and precipitation alter Reaumuria soongorica root morphology by regulating the levels of soluble sugars and phytohormones. Acta Physiol. Plant 41, 184 (2019).Article 
CAS 

Google Scholar 
Ma, X. Z. & Wang, X. P. Biomass partitioning and allometric relations of the Reaumuria soongorica shrub in Alxa steppe desert in NW China. For. Ecol. Manag. 468, 118–178 (2020).Article 

Google Scholar 
He, F. L., Bao, A. K., Wang, S. M. & Jin, H. X. NaCl stimulates growth and alleviates drought stress in the salt-secreting xerophyte Reaumuria soongorica. Environ. Exp. Bot. 162, 433–443 (2019).CAS 
Article 

Google Scholar 
Xu, D. H. et al. Photosynthetic parameters and carbon reserves of a resurrection plant Reaumuria soongorica during dehydration and rehydration. Plant Growth Regul. 60, 183–190 (2010).CAS 
Article 

Google Scholar 
Zhang, H. et al. miRNA–mRNA integrated analysis reveals roles for miRNAs in a typical halophyte, Reaumuria soongorica, during seed germination under salt stress. Plants 9, 351 (2020).CAS 
PubMed Central 
Article 

Google Scholar 
Bai, Y. M., Li, Y., Shan, L. S., Su, M. & Zhang, W. T. Effects of precipitation change and nitrogen addition on root morphological characteristics of Reaumuria soongorica. Arid Zone Res. 37, 1284–1292 (2020).
Google Scholar 
Hedwall, P. O., Nordin, A., Strengbom, J., Brunet, J. & Olsson, B. Does background nitrogen deposition affect the response of boreal vegetation to fertilization?. Oecologia 173, 615–624 (2013).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Wang, G., Fahey, T. J., Xue, S. & Liu, F. Root morphology and architecture respond to N addition in Pinus tabuliformis, west China. Oecologia 171, 583–590 (2013).ADS 
PubMed 
Article 

Google Scholar 
Grechi, I. et al. Effect of light and nitrogen supply on internal C: N balance and control of root-to-shoot biomass allocation in grapevine. Environ. Exp. Bot. 59, 139–149 (2007).CAS 
Article 

Google Scholar 
Xiao, L., Liu, G., Li, P. & Xue, S. Nitrogen addition has a stronger effect on stoichiometries of non-structural carbohydrates, nitrogen and phosphorus in Bothriochloa ischaemum than elevated CO2. Plant Growth Regul. 83, 325–334 (2017).CAS 
Article 

Google Scholar 
Quentin, A. G. et al. Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol. 35, 1146–1165 (2015).CAS 
PubMed 

Google Scholar 
White, L. M. Carbohydrate reserves of grasses: A review. J. Range Manag. 26, 13–18 (1973).CAS 
Article 

Google Scholar 
Millard, P., Sommerkorn, M. & Grelet, G. A. Environmental change and carbon limitation in trees: A biochemical, ecophysiological and ecosystem appraisal. New Phytol. 175, 11–28 (2007).CAS 
PubMed 
Article 

Google Scholar 
Zhang, T., Cao, Y., Chen, Y. M. & Liu, G. B. Non-structural carbohydrate dynamics in Robinia pseudoacacia saplings under three levels of continuous drought stress. Trees 29, 1837–1849 (2015).CAS 
Article 

Google Scholar 
Chapin, F. S., Schulze, E. D. & Mooney, H. A. The ecology and economics of storage in plants. Annu. Rev. Ecol. Syst. 21, 423–447 (1990).Article 

Google Scholar 
Sardans, J., Rivas-Ubach, A. & Peñuelas, J. The C:N: P stoichiometry of organisms and ecosystems in a changing world: A review and perspectives. Perspect. Plant Ecol. Evolut. Syst. 14, 33–47 (2012).Article 

Google Scholar 
Xia, J. Y. & Wan, S. Q. Global response patterns of terrestrial plant species to nitrogen addition. New Phytol. 179, 428–439 (2008).CAS 
PubMed 
Article 

Google Scholar 
Yang, Y. H., Luo, Y. Q., Lu, M., Schädel, C. & Han, W. X. Terrestrial C: N stoichiometry in response to elevated CO2 and N addition: a synthesis of two meta-analyses. Plant Soil 343, 393–400 (2011).CAS 
Article 

Google Scholar 
Mayor, J. R., Wright, S. J. & Turner, B. L. Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J. Ecol. 102, 36–44 (2014).CAS 
Article 

Google Scholar 
Koerselman, A. & Meuleman, A. F. The vegetation ratio: A new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33, 1441–1450 (1996).Article 

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

Google Scholar 
Wang, S., Shan, L. S., Li, Y., Zhang, Z. Z. & Ma, J. Effect of Precipitation on the Stoichiometric Characteristics of Carbon, Nitrogen and Phosphorus of Reaumuria soongarica and Salsola passerina. Acta Bot. Boreal. Occident. Sin. 40, 0335–0344 (2020).ADS 

Google Scholar 
Niu, D. C., Li, Q., Jiang, S. G., Chang, P. J. & Fu, H. Seasonal variations of leaf C:N: P stoichiometry of six shrubs in desert of China’s Alxa Plateau. Chin. J. Plant Ecol. 37, 317–325 (2013).Article 

Google Scholar 
Kleyer, M. & Minden, V. Why functional ecology should consider all plant organs: An allocation-based perspective. Basic Appl. Ecol. 16, 1–9 (2015).Article 

Google Scholar 
Yemm, E. & Willis, A. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508–514 (1954).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Bao, S. D. Soil and Agricultural Chemistry Analysis 3rd edn. (China Agriculture Press, Beijing, 2000).
Google Scholar  More

.readcube-buybox { display: none !important;}
Chocolate, a serious contender for the world’s most beloved food, is made from the seed kernels of the cacao tree (Theobroma cacao). But despite its popularity, Justine Vansynghel at the University of Würzburg in Germany and her colleagues found that nobody had quantified how species living on small-scale cacao farms collectively affect production1.

Access options

/* style specs start */
style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0 0;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50%0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:””;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
/* style specs end */Subscribe to Nature+Get immediate online access to the entire Nature family of 50+ journals$29.99monthlySubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueAll prices are NET prices.VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00All prices are NET prices.

Additional access options:

doi: https://doi.org/10.1038/d41586-022-02908-0

References

Subjects

Latest on: More

Ahmad, M., Saleem, M. A. & Sayyed, A. H. Efficacy of insecticide mixtures against pyrethroid-and organophosphate-resistant populations of Spodoptera litura (Lepidoptera: Noctuidae). Pest. Manag. Sci. 65, 266–274 (2009).CAS 

Google Scholar 
Shekhawat, S. S., Shafiq, A. M. & Basri, M. Effect of host plants on life table parameters of Spodoptera litura. Ind. J. Pure Appl. Biosci. 6, 324–332 (2018).
Google Scholar 
Sang, S. et al. Cross-resistance and baseline susceptibility of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) to cyantraniliprole in the south of China. Pest Manag. Sci. 72, 922–928 (2016).CAS 
PubMed 

Google Scholar 
Ortega, D. S., Bacca, T., Silva, A. P. N., Canal, N. A. & Haddi, K. Control failure and insecticides resistance in populations of Rhyzopertha dominica (Coleoptera: Bostrichidae) from Colombia. J. Stored Prod. Res. 92, 101802 (2021).CAS 

Google Scholar 
Li, L. Pest biological control: Goals throughout my life. Annu. Rev. Entomol. 67, 1–10 (2022).PubMed 

Google Scholar 
Razaq, M., Shah, F. M., Ahmad, S. & Afzal, M. in Pest management for agronomic crops. Agronomic Crops (ed. Hasanuzzaman M.) 365–384 (Springer, 2019).Shah, F. M. & Razaq, M. in From agriculture to sustainable agriculture: Prospects for improving pest management in industrial revolution 4.0. Handbook of Smart Materials, Technologies, and Devices: Applications of Industry 4.0. Cham. (ed. Cham) 1–18 (Springer, 2020).Razaq, M. & Shah, F. M. in Biopesticides for management of arthropod pests and weeds. Biopesticides. Biopesticides Voulme 2: Advances in Bioinoculants 7–18 (Elsevier, 2022).Kishinevsky, M., Keasar, T. & Bar-Massada, A. Parasitoid abundance on plants: Effects of host abundance, plant species, and plant flowering state. Arthropod-Plant Interact. 11, 155–161 (2017).
Google Scholar 
Islam, Y. et al. Age-stage, two-sex life table and predation parameters of Harmonia axyridis Pallas (Coleoptera: Coccinellidae), reared on Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae), at four different temperatures. Crop Prot. 2, 106029 (2022).
Google Scholar 
Furlong, M. J. & Zalucki, M. P. Climate change and biological control: The consequences of increasing temperatures on host–parasitoid interactions. Curr. Opin. Insect Sci. 20, 39–44 (2017).PubMed 

Google Scholar 
Islam, Y. et al. Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: The effect of temperature. Sci. Rep. 11, 1–13 (2021).
Google Scholar 
Keva, O. et al. Increasing temperature and productivity change biomass, trophic pyramids and community-level omega-3 fatty acid content in subarctic lake food webs. Glo. Change Bio. 27, 282–296 (2021).ADS 
CAS 

Google Scholar 
Chi, H. et al. Age-stage, two-sex life table: An introduction to theory, data analysis, and application. Entomol. Gen. 40, 103–124 (2020).
Google Scholar 
Guedes, C. Preferência alimentar e estratégias de alimentação em Coccinellidae (Coleoptera). Oecol. Aust. 17, 59–80 (2013).
Google Scholar 
Hodek, I. & Honêk, A. Ecology of coccinellidae. Vol. 54 464 (Kulver Academic Publisher, 2013).Sutherland, A. M. & Parrella, M. P. Mycophagy in Coccinellidae: Review and synthesis. Biol. Control 51, 284–293 (2009).
Google Scholar 
Hagen, K. & Ks, H. The significance of predaceous Coccinellidae in biological and integrated control of insects. Entomophaga 7, 25–44 (1974).
Google Scholar 
Jawad, D. S., Rashid, Y. D. & Hamzah, A. G. in IOP Conference Series: Earth and Environmental Science. 012029 (IOP Publishing).Kumari, S., Suroshe, S. S., Kumar, D., Budhlakoti, N. & Yana, V. Foraging behaviour of Scymnus coccivora Ayyar against cotton mealybug Phenacoccus solenopsis Tinsley. Saudi J. Biol. Sci. 28, 3799–3805 (2021).PubMed 
PubMed Central 

Google Scholar 
Alloush, A. A. Developmental duration and predation rate of the coccidophagous coccinellid Rhyzobius lophanthae (Blaisdell) (Coleoptera: Coccinellidae) on Aspidiotus nerii Bouche. Bull. Entomol. Res. 109, 612–616 (2019).PubMed 

Google Scholar 
Koch, R., Hutchison, W., Venette, R. & Heimpel, G. Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol. Control 28, 265–270 (2003).
Google Scholar 
Islam, Y., Shah, F. M., Güncan, A., DeLong, J. P. & Zhou, X. Functional response of Harmonia axyridis to the larvae of Spodoptera litura: The combined effect of temperatures and prey instars. Front. Plant Sci. 13, 849574 (2022).PubMed 
PubMed Central 

Google Scholar 
Dixon, A. F. G. & Dixon, A. E. Insect predator-prey dynamics: ladybird beetles and biological control. (Cambridge University Press, 2000).Thompson, S. Nutrition and culture of entomophagous insects. Annu. Rev. Entomol. 44, 561–592 (1999).CAS 
PubMed 

Google Scholar 
Chaudhary, D. D., Kumar, B. & Mishra, G. Functional response in Coccinellid beetles (Coleoptera: Coccinellidae) is modified by prey-density experience. Can. Entomol. 154, 55068 (2022).
Google Scholar 
Castro, C., Almeida, L. & Penteado, S. The impact of temperature on biological aspects and life table of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Fla. Entomol. 94, 923–932 (2011).
Google Scholar 
Noman, Q. M., Shah, F. M., Mahmood, K. & Razaq, M. Population dynamics of Tephritid fruit flies in citrus and mango orchards of Multan, Southern Punjab, Pakistan. Pakistan J. Zool. 54, 325–330 (2021).
Google Scholar 
Eliopoulos, P. & Stathas, G. Life tables of Habrobracon hebetor (Hymenoptera: Braconidae) parasitizing Anagasta kuehniella and Plodia interpunctella (Lepidoptera: Pyralidae): Effect of host density. J. Econ. Entomol. 101, 982–988 (2008).CAS 
PubMed 

Google Scholar 
Yu, J.-Z., Chi, H. & Chen, B.-H. Comparison of the life tables and predation rates of Harmonia dimidiata (F.) (Coleoptera: Coccinellidae) fed on Aphis gossypii Glover (Hemiptera: Aphididae) at different temperatures. Biol. Control 64, 1–9 (2013).
Google Scholar 
Roy, H. E. & Ten Brown, P. M. years of invasion: Harmonia axyridis (Pallas)(Coleoptera: Coccinellidae) in Britain. Ecol. Entomol. 40, 336–348 (2015).PubMed 
PubMed Central 

Google Scholar 
Koch, R. The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J. Insect. Sci. 3, 5689 (2003).
Google Scholar 
de Castro-Guedes, C. F., de Almeida, L. M., do Rocio, C. P. S. & Moura, M. O. Effect of different diets on biology, reproductive variables and life and fertility tables of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae). Rev. Bras. Entomol. 60, 260–266 (2016).
Google Scholar 
Abdel-Salam, A. & Abdel-Baky, N. Life table and biological studies of Harmonia axyridis Pallas (Col., Coccinellidae) reared on the grain moth eggs of Sitotroga cerealella Olivier (Lep., Gelechiidae). J. Appl. Entomol. 125, 455–462 (2001).
Google Scholar 
Islam, Y. et al. Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11, 583 (2020).PubMed Central 

Google Scholar 
Di, N. et al. Predatory ability of Harmonia axyridis (Coleoptera: Coccinellidae) and Orius sauteri (Hemiptera: Anthocoridae) for suppression of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects 12, 1063 (2021).PubMed 
PubMed Central 

Google Scholar 
Saljoqi, A.-U.-R., Khan, J. & Ali, G. Rearing of Spodoptera litura (Fabricius) on different artificial diets and its parasitization with Trichogramma chilonis (Ishii). Pak. J. Zool. 47, 1104 (2015).
Google Scholar 
Brown, P. M. et al. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, dispersal and routes of invasion. Biocontrol 56, 623–641 (2011).
Google Scholar 
Chi, H. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. Available from http://140.120.197.173/ecology/Download/TWOSEX-MSChart-B100000.rar. (2022).Chi, H. Life-table analysis incorporating both sexes and variable development rates among individuals. Environ. Entomol. 17, 26–34 (1988).
Google Scholar 
Chi, H. & Liu, H. Two new methods for the study of insect population ecology. Bull. Inst. Zool. Acad. Sin. 24, 225–240 (1985).
Google Scholar 
Goodman, D. Optimal life histories, optimal notation, and the value of reproductive value. Am. Nat. 119, 803–823 (1982).MathSciNet 

Google Scholar 
Chi, H. & Su, H.-Y. Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ. Entomol. 35, 10–21 (2006).
Google Scholar 
Tuan, S.J., Lee, C.C., Chi, H. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manag. Sci. 70, 805–813 (2014a).CAS 
PubMed 

Google Scholar 
Tuan, S.J., Lee, C.C., Chi, H. Erratum: Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manag. Sci. 70, 1936 (2014b).CAS 

Google Scholar 
Chi, H. & Yang, T.-C. Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer)(Homoptera: Aphididae). Environ. Entomol. 32, 327–333 (2003).
Google Scholar 
Chi, H. CONSUME-MSChart: a computer program for consumption rate analysis based on the age stage, two-sex life table analysis. http://140.120.197.173/ecology/Download/CONSUME-MSChart.rar. (2022).Akca, I., Ayvaz, T., Yazici, E., Smith, C. L. & Chi, H. Demography and population projection of Aphis fabae (Hemiptera: Aphididae): With additional comments on life table research criteria. J. Econ. Entomol. 108, 1466–1478 (2015).PubMed 

Google Scholar 
Akköprü, E. P., Atlıhan, R., Okut, H. & Chi, H. Demographic assessment of plant cultivar resistance to insect pests: A case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. J. Econ. Entomol. 108, 378–387 (2015).
Google Scholar 
Huang, Y. B. & Chi, H. Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci. 19, 263–273 (2012).
Google Scholar 
Wei, M. et al. Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. J. Econ. Entomol. 113, 2343–2353 (2020).PubMed 

Google Scholar 
Huang, H.-W., Chi, H. & Smith, C. L. Linking demography and consumption of Henosepilachna vigintioctopunctata (Coleoptera: Coccinellidae) fed on Solanum photeinocarpum (Solanales: Solanaceae): with a new method to project the uncertainty of population growth and consumption. J. Econ. Entomol. 111, 1–9 (2018).PubMed 

Google Scholar 
Chi, H.Timing of control based on the stage structure of pest populations: a simulation approach. J. Econ. Entomol. 83,
1143–1150 (1990).
Google Scholar 
Chi, H. TIMING-MSChart: a computer program for the population projection based on age-stage, two-sex life table. (http://140.120.197.173/Ecology/Download/TIMING-MSChart.rar). (2022).Mignault, M.-P., Roy, M. & Brodeur, J. Soybean aphid predators in Quebec and the suitability of Aphis glycines as prey for three Coccinellidae. BioControl 51, 89–106 (2006).
Google Scholar 
Brown, M. Intraguild responses of aphid predators on apple to the invasion of an exotic species, Harmonia axyridis. BioControl 48, 141–153 (2003).
Google Scholar 
Pervez, A., Chandra, S. & Kumar, R. Effect of dietary history on intraguild predation and cannibalism of ladybirds’ eggs. Int. J. Trop. Insect Sci. 41, 2637–2642 (2021).
Google Scholar 
Lundgren, J. G. Nutritional aspects of non-prey foods in the life histories of predaceous Coccinellidae. Biol. Control 51, 294–305 (2009).
Google Scholar 
Yu, J.Z. et al. Demography and mass-rearing Harmonia dimidiata (Coleoptera: Coccinellidae) using Aphis gossypii (Hemiptera: Aphididae) and eggs of Bactrocera dorsalis (Diptera: Tephritidae). J. Econ. Entomol. 111, 595–602 (2018).PubMed 

Google Scholar 
De Oliveira, R. T., dos Santos-Cividanes, T. M., Cividanes, F. J. & da Conceic, L. Harmonia axyridis Pallas (Coleoptera: Coccinellidae): Biological aspects and thermal requirements. Adv. Entomol. 2014, 5589 (2014).
Google Scholar 
Ali, S. et al. Using a two-sex life table tool to calculate the fitness of Orius strigicollis as a predator of Pectinophora gossypiella. Insects 11, 275 (2020).PubMed Central 

Google Scholar 
Merene, Y. Population dynamics and damages of onion thrips (Thripstabaci)(Thysanoptera: Thripidae) on onion in Northeastern Ethiopia. J. Entomol. Nematol. 7, 1–4 (2015).
Google Scholar 
Mou, D. F., Lee, C. C., Smith, C. & Chi, H. Using viable eggs to accurately determine the demographic and predation potential of Harmonia dimidiata (Coleoptera: Coccinellidae). J. Appl. Entomol. 139, 579–591 (2015).
Google Scholar 
Farhadi, R., Allahyari, H. & Chi, H. Life table and predation capacity of Hippodamia variegata (Coleoptera: Coccinellidae) feeding on Aphis fabae (Hemiptera: Aphididae). Biol. Control 59, 83–89 (2011).
Google Scholar 
Hance, T., van Baaren, J., Vernon, P. & Boivin, G. Impact of extreme temperatures on parasitoids in a climate change perspective. Annu. Rev. Entomol. 52, 107–126 (2007).CAS 
PubMed 

Google Scholar 
Ma, X., Zhu, J., Yan, W. & Zhao, C. Projections of desertification trends in Central Asia under global warming scenarios. Sci. Total Environ. 781, 146777 (2021).ADS 
CAS 
PubMed 

Google Scholar  More

Test animals and husbandryWild type adult zebrafish (AB line) were initially obtained from China Zebrafish Resource Center (CZRC, China) and reared at the zebrafish facility of the University of Saint Joseph, Macao. Fish were maintained in 10 L tanks in a standalone housing system (model AAB-074-AA-A, Yakos 65, Taiwan) with filtered and aerated water (pH balanced 7–8; 400–550 μS conductivity) at 28 ± 1 °C and under a 12:12 light: dark cycle. Animals were fed twice daily with live artemia and dry powder food (Zeigler, PA, USA). The fish used in this study were 6–8 months old, both males and females (1:1), with a total length of 2.2–3.1 cm. The total number of specimens tested was 30 for the auditory sensitivity measurements and inner ear morphological analysis (6 fish per experimental group), and 78 for the Novel Tank Diving assay (15-18 fish per group).All experimental procedures complied with the ethical guidelines regarding animal research and welfare enforced at the Institute of Science and Environment, University of Saint Joseph, and approved by the Division of Animal Control and Inspection of the Civic and Municipal Affairs Bureau of Macao (IACM), license AL017/DICV/SIS/2016. This study was conducted in compliance with the ARRIVE guidelines60.Noise treatmentsPrior to acoustic treatments, all subjects were transferred to 4 L isolation glass tanks that were placed in a quiet lab environment (Sound Pressure Level, SPL: ranging between 103 and 108 dB re 1 μPa) for a minimum of 7 days. These tanks had no filtering system but were subject to frequent water changes, and the light, temperature and water quality were kept similar to the stock conditions. This adaptation period was important to reduce potential effects of noise conditions from the zebrafish housing system.After this period, groups of six zebrafish were transferred into separate acoustic treatment glass tanks (dimensions: 59 cm length × 29 cm width × 47 cm height; 70 L)—Fig. 1 Supplementary, where they remained 24 h in acclimation. Each tank was equipped with an underwater speaker (UW30, Electro-Voice, MN, USA) housed between two styrofoam boards (dimensions: 3 cm thick × 29 cm width × 47 cm height) with a hole in the centre, positioned vertically in one side of the tank. Another similar sized board was positioned in the opposite side of the tank and fine sand was placed in the bottom to minimize transmission of playback vibrations into the tank walls. Each treatment tank was mounted on top of styrofoam boards placed over two granite plates spaced by rubber pads to reduce non-controlled vibrations.Four acoustic treatment tanks were prepared for this study to be used alternately between trials and cleaning procedures, but only two were used simultaneously. When two tanks were being used, one contained specimens under acclimation and the other fish under a specific acoustic treatment. The tanks were housed in a custom-made rack and placed at least 1 m apart to minimize acoustic interferences. The tanks were used randomly for the different treatments across the various trials.The speakers were connected to audio amplifiers (ST-50, Ai Shang Ke, China) that were connected to laptops running Adobe Audition 3.0 for windows (Adobe Systems Inc., USA). After the acclimation period, specimens were exposed to white noise playbacks (bandwidth: 100–3000 Hz) at 150 dB re 1 µPa for 24 h, starting in the morning between 10 and 11 a.m. The bandwidth adopted covered the best hearing range of zebrafish27, as well as the frequency range of most anthropogenic noise sources, such as pile driving and vessels2.Sound recordings and SPL measurements were made with a hydrophone (Brüel & Kjær type 8104, Naerum, Denmark; frequency range: 0.1 Hz–120 kHz, sensitivity of − 205 dB re 1 V/μPa) connected to a hand-held sound level meter (Brüel & Kjær type 2270). Noise level was adjusted with the speaker amplifier so that the intended amplitude (LZS, RMS sound level obtained with slow time and linear frequency weightings: 6.3 Hz–20 kHz) was achieved at the centre of the tanks before each treatment. A variation in SPL of ±10 dB was registered in the closest and farthest points (in relation to the speaker). The sound spectra of the noise treatments were relatively flat similar to the setup described in a prior study by Breitzler et al.27.Moreover, the acoustic treatments were calibrated with a tri-axial accelerometer (M20-040, frequency range 1–3 kHz, GeoSpectrum Technologies, NS, Canada) with the acoustic centre placed in the middle of the tank. The sound playback generated was about 120 dB re 1 m/s2, with most energy in the horizontal axis perpendicular to the speaker, which was verified based on previously described methods using a MATLAB script paPAM16.In this study four sound treatments were used with varying temporal patterns similar to Sabet et al.18—Fig. 1: continuous noise (CN); intermittent regular noise with a fast pulse rate—1 s pulses interspersed with 1 s silence (IN1,1); intermittent regular noise with a slow pulse rate—1 s pulses interspersed with 4 s silence (IN1,4) and intermittent random noise—1 s pulses interspersed with 1, 2, 3, 4, 5, 6 or 7 s silent intervals in randomized sequence (RN1,7) leading to a mean interval of 4 s. All intermittent patterns had 5 ms ramps to fade in and fade out pulses for smooth transitions. In the “control” treatment tank, the amplifier connected to the speaker was switched on but without playback.After each treatment, two specimens were tested for audiometry, two were tested with the NTD assay and another two were euthanized and dissected for inner ear morphological analysis.Auditory sensitivity measurementsAuditory Evoked Potential (AEP) recordings were conducted immediately after noise treatments. The AEP recording technique adopted followed previously described procedures27. The recordings were conducted in a rectangular plastic tank (50 cm length × 35 cm width × 23 cm height) equipped with an underwater speaker (UW30) positioned in the bottom and surrounded by fine sand. A custom-built sound stimulation system with enhanced performance at lower frequencies ( More

Acidification of CPHistorical geochemical data suggest that the water chemistry of Cinder Pool (CP) has been relatively stable from the time of first reported geochemical data in 1947 until autumn 2018, followed by pronounced acidification between winter and spring 2019 (Supplementary Data 1, Fig. 1a, b). Images and documentation dating to even earlier (1927) reveal the presence of cinders covering ~50% of the spring surface at that time, a temperature near boiling (91.5 °C), and a description of having high sulfate and chloride levels (although data was not provided), suggesting that its chemistry has been generally stable since its discovery1. Spring pH ranged between ~3.6 and 4.5 in 22 yearly measurements spanning 71 years (1947–2018; multiple measurements in the same year were averaged to represent each year) (Fig. 1b), while the pH has been subsequently measured after 2018 as low as 2.5 (Fig. 1b). A single pH measurement of 2.5 was also recorded in a 2003 publication27, although other measurements in 2003, 2000, and 2001 were more consistent with the long-term average (i.e., pH 4.2–4.3; Supplementary Data 1). Scrutiny of chemical data accompanying the pH 2.5 measurement in 2003 indicates a SO42− concentration (~48 mg L−1) that is considerably lower than would be expected for CP, even when the pH is much higher (SO42− = 80 mg L−1; pH = 4.2–4.3). Considering that sulfuric acid is the predominant buffer of pH in these systems7,28, the pH 2.5 reading in 2003 is considered questionable. Nevertheless, the 2018 shift in pH towards more acidic conditions was accompanied by a notable change in the appearance of CP. Prior to autumn 2018, the spring waters were cloudy gray with the considerable suspension of kaolinite clay particles20 and black cinders10. However, between autumn 2018 and spring 2019, the spring waters visibly turned blue-green and contained colloidal S° particles that were also deposited along the pool shelves, while the pool also lacked its characteristic black cinders (Fig. 1a). The spring has maintained this appearance since spring 2019 until at least July 2022.Fig. 1: Historical geochemistry of Cinder Pool (CP).a Top panel shows the visual change in the appearance of CP in 2016 (left) and 2020 (right). Scale bars in the bottom right are ∼1 m. b Measurements of pH (n = 21; black line) and sulfate (SO42−) concentrations (n = 12; red line) in CP waters between 1947 and 2021. Years with multiple measurements were averaged to represent the entire year. c Paired measurements of SO42− and chloride (Cl−) concentrations (n = 12) between 1947 and 2021 in the context of the same measurements for 488 YNP springs derived from previous studies. Paired points for CP are colored based on the year they were recorded (averaged for multiple measurements/year as described above). End member fluid compositions as described in the manuscript text are indicated based on the abbreviations: MO meteoric only, HO hydrothermal only, MG meteoric plus gas, HB hydrothermal plus boiling, HBG hydrothermal plus boiling plus gas. Points for 2016, 2018, 2019, 2020, and 2021 are indicated by “16”, “18”, “19”, “20”, and “21”, respectively.Full size imageThe source of fluids in YNP hot springs can be broadly defined by concentrations of sulfate (SO42−) and chloride (Cl−)2,7. These indicators have been previously used to define the source of YNP springs as either (1) hydrothermal only (HO) waters that have moderate concentrations of SO42− (~30 mg L−1 depending on the depth of boiling; described below) but high concentrations of Cl− (~300 mg L−1), (2) meteoric-only (MO) waters containing lower concentrations of both solutes, or (3) MO waters infused with gas (MG) that have lower Cl− concentrations and higher SO42− concentrations (Fig. 1c). Subsequent boiling and/or evaporation of HO waters can concentrate Cl− and SO42− to higher concentrations (termed hydrothermal plus boiling; HB), while additional gas input into HO or HB waters can lead to particularly high concentrations of both Cl− and SO42− (hydrothermal + boiling + gas; HBG)7 (Fig. 1c). Geochemical data from surveys spanning 1947 to 2018 suggest that CP was largely sourced by hydrothermal (HO) waters that have undergone boiling and/or evaporation (HB) during this time frame (Fig. 1c).HO and HB waters are typically circumneutral7, while CP (which is also sourced by HB waters) has maintained a moderately acidic pH of ~4 until autumn 2018 (Fig. 1b). Several other low pH HB waters have been previously observed within the NGB7. The moderately acidic pH in CP (prior to 2018) has been attributed to the hydrolysis of molten S° that occurs at depths of >18 m that leads to the formation of S2O32– 11. Oxygen (O2)-dependent oxidation of S2O32−, catalyzed by trace iron sulfide in the cinders, forms SxO62− that can then react with sulfide to yield S2O32− and S° 11. Alternatively, SxO62− can be disproportionated to form S2O32− and SO42− 11. The relative rates of these reactions in CP prior to 2018 are not known although similar concentrations of S2O32− measured between 1995 and 1997 suggest that rates of S° hydrolysis and rates of S2O32− formation have been relatively constant over yearly time scales11. The consumption of O2 by reaction with S2O32− and the consumption of sulfide involving reactions with SxO62− would limit the amount of sulfuric acid that could be formed, thereby maintaining a less acidic pH than other sulfuric acid buffered acidic springs in YNP7.Between November 2018 and March 2019, the pH of CP markedly decreased to 2.8 in 2019, 2.7 in 2020, and 2.6 in 2021. This coincided with a marked increase in SO42− concentrations of ~3–5 fold above historical ranges (Fig. 1b), while Cl− concentrations fluctuated without clear trends during this time (Supplementary Fig. 1c). Thus, CP transitioned from an HB water type to an HBG water type between autumn 2018 and spring 2019 and has remained this way since (Fig. 1c). This is interpreted to reflect a substantial increase in H2S/S° oxidation that results in the formation of SO42− and H+ (sulfuric acid). Several observations suggest a fundamental restructuring of CP’s unique sulfur cycling due to dramatic physical and chemical changes at this time. As described in more detail below, the molten S° layer was detected at a depth of 18 m in 2016. However, in 2020 and 2021 there was no evidence of molten S° at ~18 to 20 m depth as previously documented, and sampling equipment could be freely dropped to a depth of 22 m (length of the cable) without interruption. In the absence of the molten S° at depth, the S° hydrolysis product S2O32−, and the cinders that catalyze SxO62− formation from S2O32− and H2S, it is possible that such reactions that previously competed for H2S or O2 (i.e., those involving S2O32− and SxO62−) are no longer taking place in CP. This in turn would allow for sulfur compounds (H2S and S°) to now be oxidized, thereby contributing to spring acidification.Alternative scenarios underlying the dramatic changes in CP waters also warrant consideration, and the three most logical are presented below. First, it is possible that the waters sourcing CP may have shifted either via replacement of the primary source or by altered mixing of multiple water sources. Water isotope values (δ2H and δ18O) can be used to further deconvolute the sources of hydrothermal waters because distinctive isotope values are associated with distinct water sources and the various influences upon them including meteoric water recharge, boiling (and/or evaporation), and water–rock interactions7,29. The water isotope values measured among the measured depths in CP in 2020 were near the range of water isotope values observed in CP across multiple months in 201613 (depth-resolved water isotope measurements were not made in 2016). The 2020 CP water isotope values were slightly right-shifted relative to those of 2016, suggesting a minor increase in the evaporation and concentration of CP water isotopes between 2016 and 20207 (Supplementary Fig. 2). These data thus do not support the hypothesis that the source of waters in CP dramatically shifted between 2016 and 2020, consistent with the SO42− and Cl− measurements indicating that the primary change to CP waters was increased input or availability of H2S for oxidation.A second alternative explanation is that a change in the water level of CP could potentially alter residence times which could allow for more oxidation of sulfur compounds in the spring and increased acidification. Such a scenario would also likely result in increased evaporation and concentration of solutes. However, the minimal increase in water isotope values (Supplementary Fig. 2) and similar Cl− concentrations (Supplementary Fig. 1c) accompanying a ~3–5 fold increase in SO42− concentration pre- and post-acidification (Fig. 1b) argue that increased residence time was of minimal importance in acidification.A third possible explanation is that a change in the plumbing system of CP is now delivering more vapor phase gas that contributes H2S and acidity when oxidized. Such a scenario could be consistent with increased surface deformation, subsurface gas accumulation, and seismic activity that has been taking place near NGB just prior to these changes21, and the transition from HB-type to HBG-type waters in CP. Sulfur species isotope analyses would help deconvolute the sources of SO42− in CP, but samples for sulfur isotopic analyses were not collected prior to acidification. Thus, it is unclear if this process may also be contributing to the acidification of CP. Regardless, the disappearance of the molten S° cap either by consumption or displacement would in effect make H2S more available for oxidation, similar to increased vapor phase input. The acidification of hot springs involves the oxidation of H2S by O230. More specifically, partial oxidation of H2S at acidic pH (90% amino acid identity to other homologs from UYS MAGs), but that was only present on unbinned contig sequences. Proteins are grouped based on their functionalities and associations in complexes. TetH (tetrathionate hydrolase), SQO sulfide:quinone oxidoreductase, SOR sulfur oxygenase reductase, SoxABCD Sulfolobus oxidase, SoxM Sulfolobus oxidase, CbsAB cytochrome b 558/566, SoxLN cytochrome ba complex, DoxBCE Desulfurolobus oxidase, DoxAD/TQOab Desulfurolobus oxidase/thiosulfate-quinone oxidoreductase, HdrAB1C1B2C2 (heterodisulfide reductase), DsrE3 DsrE3 sulfurtransferase, Dld dihydrolipoamide dehydrogenase, LplA lipoate-protein ligase A, LbpA lipoate binding protein A/glycine cleavage system H protein, TusA tRNA 2-thiouridine synthesizing protein A, SreABC sulfur reductase, SAOR sulfite:acceptor oxidoreductase, HcaLS [NiFe]-hydrogenase group 1 g. SoxEFGHI and FoxABCDEFGH (ferrous iron oxidation) gene sets were also investigated, but not identified in any of the MAGs and not shown here for brevity. A complete description of the enzymes/proteins found in individual UYS MAGs is provided in Supplementary Data 4.Full size imageTo assess the potential role of the UYS in sulfur biogeochemical cycling, the metabolic functional potentials of these populations were evaluated in greater detail based on their reconstructed genomes (Fig. 5, Supplementary Data 3). The UYS encoded the capacity for autotrophy via full complements of enzymes involved in the 3-hydroxypropionate/4-hydroxybutyrate cycle (3HP-4HB) (Supplementary Data 4), consistent with the general potential for autotrophy in most other Sulfolobales36. Consistently, the SoxM subunit that has been suggested as a marker for (facultatively) heterotrophic growth of Sulfolobales37 was absent in all UYS MAGs (Fig. 5, Supplementary Data 4). Given that all known Acidilobus and Vulcanisaeta spp. are characterized heterotrophs without known autotrophic capacity38,39, the UYS are likely the sole primary producers in the CP surface and subsurface waters, consistent with their considerable dominance in CP water communities over time.Also consistent with almost all other Sulfolobales36, the UYS universally encode the ability to reduce O2 via terminal cytochrome oxidases, although not via Sulfolobus oxidase (SoxABCD) complexes that are common among many Sulfolobales36 but rather via Desulfurolobus oxidase complexes (DoxBCE) (Fig. 5, Supplementary Data 4). An additional terminal oxidase complex (CbsAB-SoxLN) was encoded in the 2020 CP MAGs along with several other UYS MAGs from other YNP springs, although homologs of CbsAB-SoxLN were not present in the 2016 CP MAGs or several others recovered from sediments of other hot springs (Fig. 5). Thus, a potentially important metabolic difference between the pre- and post-acidification (2016 and 2020, respectively) CP Sulfolobales was the ability to use different terminal cytochrome oxidase compliments for aerobic respiration. The capacity to use multiple terminal oxidases has been suggested as an adaptation to varying oxygen tensions/availabilities37,40 that likely substantively differed between the low ORP 2016 CP waters and the high ORP 2020 CP waters (Fig. 2c). Consequently, these data point to the ecological succession of UYS strains within CP that are, at least in part, related to strain-level differences in aerobic respiration capacities.A defining feature of most cultured Sulfolobales is the ability to grow chemolithoautotrophically by coupling the oxidation of sulfur compounds (e.g., S0) to aerobic respiration37. The slow kinetics associated with abiotic oxidation of S0 with O2 at temperatures More

Intra-bull semen quality variationTo understand variation in bull semen quality, we assessed 1271 ejaculates from 79 different bulls (11 different breeds) housed at Rockhampton stud farm, in the state of Queensland, Australia, over a period of 5 years (2014–2018). The raw data, together with the semen analysis and when the samples for each individual bull were collected is available in Supplementary 1. The climate in this area (23.3786° S, 150.5089° E) is considered sub-tropical, ranging from 16 °C in winter to over 30 °C in summer. A comprehensive semen analysis was undertaken, including sperm morphology and motility. To determine the variation in semen quality, we plotted the percentage of sperm normal forms for each bull that had 5 or more ejaculates taken annually. Morphology was used as a measure of sperm quality, as Söderquist et al.17 demonstrated that sperm motility is heavily influenced by the collection/collectors and, therefore potentially unreliable and irreproducible. This resulted in the analysis of 1178 ejaculates from 50 bulls, with an average of 23 ejaculates per bull. The percentage of sperm normal forms as a box and whiskers plot for each bull is given (Fig. 1). As shown, many bulls demonstrated extremely high variation between ejaculates, with several males ranging from  70% (considered an outright “pass” in terms of cryopreservation potential) of normal sperm morphology. On the contrary, some bulls appeared to produce consistent semen samples across the year.Figure 1Changes in sperm normal forms. Semen samples were taken from bulls via electroejaculation and the percentage sperm normal forms were counted. The data show a box and whiskers plot consisting of 50 bulls, each of which had at least 5 different ejaculates across a minimum one month. Each box and whiskers plot represents an individual Bull showing the median, upper and lower quartile range. Outliers are represented by individual dots.Full size imageTo determine the amplitude and the proportion of bulls demonstrating variation in the number of normal sperm forms, we measured the difference between the maximum and the minimum values recorded for each animal. From this analysis we found that: 9 (18%) bulls showed less than 20% variation in normal forms; 15 (30%) bulls had between 20–40% variation; 13 (26%) bulls were between 40–60% and for 13 (26%) bulls this number was over 60%. These data have major implications when interpreting semen analysis, since a bull could be classified as either fertile or infertile depending on which ejaculate was considered. This data also sheds light into why correlations between the vBBSE parameters such as morphology and the bull fertility are so variable.Seasonal effect on semen qualitySeveral sources of environmental influence have been suggested to affect bull sperm quality. These include feed availability (i.e., higher conception rates in rainy seasons)27, excessive protein intake28, day length29, thermal heat stress and age30,31. To better understand the dynamics of semen quality variation within our samples, we plotted sample “pass” and “fail” cryopreservation criteria against the month of collection. A raw bull semen sample is classified as “pass” when motility is above 60% and normal forms greater than 70%. When samples were between 30 and 60% motility and 50–70% normal forms, they were classified as a “compensatory” (or qualified) pass (q-pass). The compensatory pass relied on there being the ability to have at least 10 million motile normal forms of spermatozoa in each straw to allow for conception. An outright failure was given to any sample with less than 30% progressive motility or 50% normal forms. This allowed each ejaculate to be placed into a binary “pass” or “fail”.The data for the percentage of total males that “failed” within each month (1271 ejaculates) is shown (Fig. 2A). Clearly, there is a seasonal pattern, with over 90% pass rate in winter (June–August) that fell to 50% or lower in summer (Dec-Feb). Considering that all bulls were greater than 4 years old, housed on the same stud farm and received the same dietary supplement we found no relationship in terms of “pass” or “fail” rates to these parameters. Thus, the data clearly suggested that Temperature/Temperature-Humidity or day length were responsible for the increased failure rates seen during Summer. Therefore, to understand if there was any causal relationship, we correlated either the average monthly temperature (Fig. 2B) or daylight (Fig. 2C) with monthly failure rates. The data showed a correlation with monthly temperature (r2 = 0.55; and temperature-humidity index – see further modelling below) but not with daylight hours (r2 = 0.05). Combined, these data suggest that temperature was the most likely reason for increased failure rates during the warm/hot months.Figure 2Seasonal variation in the semen quality of 1271 bull semen ejaculates. Semen samples were taken from bulls via electroejaculation and a full semen analysis was undertaken. Each sample was then classified as a pass or fail as described in Materials and Methods. (A) The percentage failure rate for each month is shown for all bulls. The number above each column indicate how many semen ejaculates were processed that month. (B). Scatter plot showing the average monthly temperature of Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.55. (C) Scatter plot showing the average daily sunlight in Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.04.Full size imageChanges in normal sperm forms categorised by breedThe present study investigated 11 different breeds of cattle, and we reasoned that maybe one, or more breed(s) contributed to failure rates more than others. Therefore, we plotted the percentage of normal forms for every ejaculate against the breed (Fig. 3). All breeds showed similar variation except for the Belmont Red, Boran and Wagyu. However, a relatively small number of bulls from the Belmont Red and Boran breeds were assessed in this study, therefore, it is unclear if they are indeed more resistant to heat. In the case of the Wagyu, it is worth mentioning that only one animal exhibited poor sperm morphology in several ejaculates (Fig. 3 circled) during winter. A close inspection of the records showed that during this time the animal had a fever episode, with body temperature reaching 39.4 °C, and that the sperm morphology returned to normal in approximately 70 days.Figure 3Variation in Semen quality as judged by Bull breed. Semen sample was collected and analysed for sperm morphology. The animals were then separated according to breed and the percentage normal forms for each ejaculate are shown.Full size imageSome bulls are heat-sensitive, whilst others are heat-tolerantAnalysis of the present data clearly illustrated that some bulls showed marked variation in terms of their semen quality throughout the year (Fig. 1). Meanwhile, others demonstrated much less variation, and were reasonably consistent. To further clarify these differences, we closely analysed the percentage of sperm morphology from two bulls, both of whom had several ejaculates were taken throughout the year, including during and after summer (Fig. 4). There was a clear pattern, and evidence of two types of bulls. Prior to the summer season, bull 1 (Fig. 4, red), designated here as “heat-sensitive”, exhibited  > 70% normal forms of spermatozoa. This value decreases dramatically, reaching its lowest point (10%) mid-January, before undergoing a recovery by April ( > 70%). In contrast, bull 2 (Fig. 4, green) showed a consistent semen profile throughout the year. The data suggest this bull was more “heat-tolerant”.Figure 4Identification of Heat-Sensitive and Heat-Tolerant bulls. The percentage normal sperm morphology from two bulls, both Droughtmasters, which had several ejaculates taken over the course of the year were plotted against the month in which the semen sample was taken. The first bull (red) is an example of a heat-sensitive bull. The second bull (Green) an example of heat-tolerant response.Full size imageTo further explore the concept of “heat-tolerant” and “heat-sensitive” bulls, we subjected 20 Wagyu bulls to a single event of controlled heat stress (40 °C, 12 h). This experiment was performed during Winter, at Singleton (New South Wales, Australia, 32.5695° S, 151.1788° E), where the average temperature was 17 °C and never exceeded 18 °C. Prior to the heat stress event, baseline semen samples were taken from each animal. After heat stress, semen samples were taken every week for 11 weeks. During the experiment, two bulls were removed from the program due to infection and sickness whilst a 3rd bull was removed as it refused to co-operate with electroejaculation procedure. From the remaining bulls, we were able to reproduce the heat-sensitive and heat-tolerant bull phenomenon. The raw data from this work is given in Supplementary 1, and an example of the data is shown (Fig. 5). For 14 bulls, we found no difference in terms of their baseline samples, which were between 70–90% normal forms. This is consistent with the Wagyu bull characteristics and their heat-tolerance (Fig. 5, yellow, green, blue lines). Within these “heat-tolerant” bulls, there was a variation of 16–22% sperm normal forms. For the other three bulls, two of them showed a decline in sperm quality, which began 2–3 weeks after the heat event, dropping from a baseline of 85% and 90% normal forms to 55% and 59%, respectively (30–31% variation in normal forms; Fig. 5, grey and orange line). The third bull showed a greater degree of heat-sensitivity. Starting at 77% morphologically normal sperm, the spermiogram of this bull illustrated a rapid decrease in normal forms in a short time (2 weeks), reaching around 40% after 4–5 weeks. Sperm morphology remained at this level (37% variation in normal form) for four weeks, before recovery. These data show that under experimental condition, the phenomenon of heat-sensitive and heat-tolerant animals can be reproduced. Further, it appears that there are degrees of heat-sensitivity.Figure 5Heating of Wagyu bulls to identify heat-sensitive and heat-tolerant effect. Twenty Wagyu bulls all 3 years of age and over were heated to 40 °C for 12 h in an insulated barn. Before heating, bassline samples were taken (week 1). After heating, electroejaculation was used to collect semen every week for 11 weeks. For every sample, sperm morphology was counted by a qualified theriogenologist. The data show the percentage normal morphology for 5 bulls. The light blue line indicates a heat-sensitive bulls, whose morphology was affected by heat, then returned back to baseline. The orange and grey line represent two related bulls (same father) who also produced less than 70% normal forms. The yellow, green and dark blue lines represent three heat-tolerant bulls, whose semen profile did not drop below the 70% normal spermatozoa threshold.Full size imageEnvironmental heat stress leads to poor sperm quality 17 days laterSimilar to previous reports, we noted that sperm quality does not begin to deteriorate until 2–3 weeks after the heat stress event of the bulls32. Based on the timing of spermatogenesis, this is consistent with reports that meiotic cells are more susceptible to heat stress following a heating event, with poor quality spermatozoa appearing in the ejaculate around 2–3 weeks later. To better understand the relationship between a “heat-event” and the production of poor-quality spermatozoa, we modelled both maximum temperature and maximum temperature humidity index (THI) and their relationship to the proportion of morphologically normal spermatozoa. The THI is an index representing the effect of humidity on the heat stress of an animal. THI was obtained using the following formula:$$mathrm{THI}=0.8* frac{{T}_{max}}{100}+frac{left(humidity*left({t}_{max}-14.4right)right)}{1}+46.4$$where Tmax = maximum temperature, (oF), and H = relative humidity.We plotted the correlation between semen quality and Tmax on the day, and every day prior (up to 40 days) to semen collection (Fig. 6). This modelling demonstrated that poor semen quality was due to maximum daytime temperature 17 days prior (Fig. 6a, arrow). Notably, 1 day of heat-stress appears to be sufficient to cause poor sperm quality, since if we take the average of 2 (Fig. 6b) or 3-day maximal temperatures prior to collection (Fig. 6c) the correlation patterns were similar. Supplementary 3 shows further modelling for Tmax and THI using between 1 and 5-day average temperatures prior to semen collection.Figure 6Bull semen quality (as percentage sperm normal forms) is related to the temperature that occurred 17–19 days ago. Correlation between sperm quality and maximum Temperature (Tmax). The Y axis is the Pearson correlation coefficient and X axis represents the number of days before the day the sperm sample was taken. (a) Uses one day of Tmax data whilst (b) averages two and (c) averages three consecutive days of Tmax data. The arrow shows the best correlation between Tmax and poor sperm quality, which occurs around 17–19 days before the semen sample is collected.Full size imageUnderstanding the temperatures at which heat-sensitive bulls failTo determine the Tmax at which bulls in the paddock begin to produce poor quality spermatozoa, we modelled data using both parameters measured at 17 days prior to the heat event, and plotted samples from 12 heat-sensitive bulls (6 Brahmans, 4 Drought Masters and 2 Santa Gertrudis). The relationship between sperm morphology and Tmax 17 days prior to heat even was plotted, with a spline smoothing cure to show the mean quality as a function of Tmax (Fig. 7a). As the temperature increase, so the quality of sperm morphology decreases as expected. To gain further clarity, we next fitted a nominal logistic regression analysis to model the proportion of spermatozoa that would either pass, Q-pass or fail sperm cryopreservation criteria as a function of Tmax 17 days prior. Tmax effect was highly significant for both outcome categories, with both p  More