More stories

  • in

    The role of epiphytes in seagrass productivity under ocean acidification

    Cullen-Unsworth, L. C. et al. Seagrass meadows globally as a coupled social-ecological system: Implications for human wellbeing. Mar. Pollut. Bull. 83, 387–397 (2014).CAS 
    Article 

    Google Scholar 
    Ondiviela, B. et al. The role of seagrasses in coastal protection in a changing climate. Coast. Eng. 87, 158–168 (2014).Article 

    Google Scholar 
    Campagne, C. S., Salles, J.-M., Boissery, P. & Deter, J. The seagrass Posidonia oceanica: ecosystem services identification and economic evaluation of goods and benefits. Mar. Pollut. Bull. 97, 391–400 (2015).CAS 
    Article 

    Google Scholar 
    Boudouresque, C. F., Mayot, N. & Pergent, G. The outstanding traits of the functioning of the Posidonia oceanica seagrass ecosystem. Biol. Mar. Medit. 13, 109–113 (2006).
    Google Scholar 
    Duarte, C. M., Kennedy, H., Marbà, N. & Hendriks, I. Assessing the capacity of seagrass meadows for carbon burial: Current limitations and future strategies. Ocean Coast. Manag. 83, 32–38 (2013).Article 

    Google Scholar 
    Barrón, C., Duarte, C. M., Frankignoulle, M. & Borges, A. V. Organic carbon metabolism and carbonate dynamics in a mediterranean seagrass (Posidonia oceanica) Meadow. Estuar. Coasts 29, 417–426 (2006).Article 

    Google Scholar 
    Marbà, N., Díaz-Almela, E. & Duarte, C. M. Mediterranean seagrass (Posidonia oceanica) loss between 1842 and 2009. Biol. Conserv. 176, 183–190 (2014).Article 

    Google Scholar 
    Chefaoui, R. M., Duarte, C. M. & Serrão, E. A. Dramatic loss of seagrass habitat under projected climate change in the Mediterranean Sea. Glob. Chang. Biol. 24, 4919–4928 (2018).ADS 
    Article 

    Google Scholar 
    Marbà, N. & Duarte, C. M. Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Glob. Chang. Biol. 16, 2366–2375 (2010).ADS 
    Article 

    Google Scholar 
    Lovelock, C. E. et al. Assessing the risk of carbon dioxide emissions from blue carbon ecosystems. Front Ecol Env. 15, 257–265 (2017).Article 

    Google Scholar 
    Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Chang. Biol. 19, 1884–1896 (2013).ADS 
    Article 

    Google Scholar 
    Zunino, S., Libralato, S., Canu, D. M., Prato, G. & Solidoro, C. Impact of ocean acidification on ecosystem functioning and services in habitat-forming species and marine ecosystems. Ecosystems https://doi.org/10.1007/s10021-021-0060 (2021).Article 

    Google Scholar 
    Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407, 364–367 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: the other CO2 problem. Annu. Rev. Mar. Sci. 1, 169–192 (2009).ADS 
    Article 

    Google Scholar 
    Koch, M., Bowes, G., Ross, C. & Zhang, X.-H. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Chang. Biol. 19, 103–132 (2013).ADS 
    Article 

    Google Scholar 
    Zimmerman, R. C. et al. Experimental impacts of climate warming and ocean carbonation on eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 566, 1–15 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    Egea, L. G., Jimé Nez-Ramos, R., Herná Ndez, I., Bouma, T. J. & Brun, F. G. Effects of ocean acidification and hydrodynamic conditions on carbon metabolism and dissolved organic carbon (DOC) fluxes in seagrass populations. PLoS ONE https://doi.org/10.1371/journal.pone.0192402 (2018).Article 

    Google Scholar 
    Jiang, Z. J., Huang, X.-P. & Zhang, J.-P. Effects of CO 2 enrichment on photosynthesis, growth, and biochemical composition of seagrass thalassia hemprichii (ehrenb.) aschers. J. Integr. Plant Biol. 52, 904–913 (2010).CAS 
    Article 

    Google Scholar 
    Apostolaki, E. T., Vizzini, S., Hendriks, I. E. & Olsen, Y. S. Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent. Mar. Environ. Res. 99, 9–15 (2014).CAS 
    Article 

    Google Scholar 
    Hendriks, I. E. et al. Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11, 333–346 (2014).ADS 
    Article 

    Google Scholar 
    Bergstrom, E., Silva, J., Martins, C. & Horta, P. Seagrass can mitigate negative ocean acidification effects on calcifying algae. Sci. Rep. 9(1), 1–11 (2019).CAS 
    Article 

    Google Scholar 
    Hernán, G. et al. Seagrass (Posidonia oceanica) seedlings in a high-CO 2 world: from physiology to herbivory. Sci. Rep. 6(1), 1–12 (2016).MathSciNet 
    Article 

    Google Scholar 
    Cox, T. E. et al. Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity. J. Ecol. 103, 1594–1609 (2015).CAS 
    Article 

    Google Scholar 
    Cox, T. E. et al. Effects of in situ CO2 enrichment on structural characteristics, photosynthesis, and growth of the Mediterranean seagrass Posidonia oceanica. Biogeosciences 13, 2179–2194 (2016).ADS 
    Article 

    Google Scholar 
    Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454(7200), 96–99 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    Mecca, S., Casoli, E., Ardizzone, G. & Gambi, M. C. Effects of ocean acidification on phenology and epiphytes of the seagrass Posidonia oceanica at two CO2 vent systems of Ischia (Italy). Mediterr. Mar. Sci. 21, 70–83 (2020).Article 

    Google Scholar 
    Ugarelli, K., Chakrabarti, S., Laas, P. & Stingl, U. The seagrass holobiont and its microbiome. Microorganisms 5(4), 81 (2017).Article 

    Google Scholar 
    Tarquinio, F., Hyndes, G. A., Laverock, B., Koenders, A. & Säwström, C. The seagrass holobiont: understanding seagrass-bacteria interactions and their role in seagrass ecosystem functioning. FEMS Microbiol. Lett. 366, 1–15 (2019).Article 

    Google Scholar 
    Brodersen, K. E. & Kühl, M. Effects of Epiphytes on the Seagrass Phyllosphere. Front. Mar. Sci. 9, 1–10 (2022).Article 

    Google Scholar 
    Seymour, J. R., Laverock, B., Nielsen, D. A., M., T.-T. S. & Macreadie, P. I. The Microbiology of Seagrasses. in Seagrasses of Australia 343–392 (Springer International Publishing, 2018). https://doi.org/10.1007/978-3-319-71354-0Ruocco, N. et al. First evidence of Halomicronema metazoicum (Cyanobacteria) free-living on Posidonia oceanica leaves. PLoS ONE 13(10), e0204954 (2018).Article 

    Google Scholar 
    Kohn, T. et al. The microbiome of posidonia oceanica seagrass leaves can be dominated by planctomycetes. Front. Microbiol 11, 1458 (2020).Article 

    Google Scholar 
    Casola, E., Scardi, M., Mazzella, L. & Fresi, E. Structure of the epiphytic community of posidonia oceanica leaves in a shallow meadow. Mar. Ecol. 8, 285–296 (1987).ADS 
    Article 

    Google Scholar 
    Martin, S. et al. Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol. Lett 4, 689–692 (2008).Article 

    Google Scholar 
    Foo, S. A., Byrne, M., Ricevuto, E. & Gambi, M. C. The carbon dioxide vents of Ischia, Italy, a natural system to assess impacts of ocean acidification on marine ecosystems: an overview of research and comparisons with other vent systems. Oceanogr. Mar. Biol. 56, 237–310 (2018).
    Google Scholar 
    Olivé, I., Silva, J., Costa, M. M. & Santos, R. Estimating seagrass community metabolism using benthic chambers: the effect of incubation time. Estuaries Coasts 39, 138–144 (2016).Article 

    Google Scholar 
    Barrón, C. & Duarte, C. M. Dissolved organic matter release in a Posidonia oceanica meadow. Mar. Ecol. Prog. Ser. 374, 75–84 (2009).ADS 
    Article 

    Google Scholar 
    Langsrud, Ø. ANOVA for unbalanced data: Use Type II instead of Type III sums of squares. Stat. Comput. 13, 163–167 (2003).MathSciNet 
    Article 

    Google Scholar 
    RStudio Team. RStudio. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. (2021).Donnarumma, L., Lombardi, C., Cocito, S. & Gambi, M. C. Settlement pattern of Posidonia oceanica epibionts along a gradient of ocean acidification: an approach with mimics. Mediterr. Mar. Sci. 15, 498–509 (2014).Article 

    Google Scholar 
    Gravili, C., Cozzoli, F. & Gambi, M. C. Epiphytic hydroids on Posidonia oceanica seagrass meadows are winner organisms under future ocean acidification conditions: evidence from a CO2 vent system (Ischia Island, Italy). Eur. Zool. J. 88, 472–486 (2021).CAS 
    Article 

    Google Scholar 
    Rodolfo-Metalpa, R., Lombardi, C., Cocito, S., Hall-Spencer, J. M. & Gambi, M. C. Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar. Ecol. 31, 447–456 (2010).CAS 

    Google Scholar 
    Wear, D. J., Sullivan, M. J., Moore, A. D. & Millie, D. F. Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Mar. Ecol. Prog. Ser. 179, 201–213 (1999).ADS 
    Article 

    Google Scholar 
    Hasegawa, N., Hori, M. & Mukai, H. Seasonal shifts in seagrass bed primary producers in a cold-temperate estuary: Dynamics of eelgrass Zostera marina and associated epiphytic algae. Aquat. Bot. 86, 337–345 (2007).Article 

    Google Scholar 
    Piazzi, L., Balata, D. & Ceccherelli, G. Epiphyte assemblages of the Mediterranean seagrass Posidonia oceanica: an overview. Mar. Ecol. 37, 3–41 (2016).ADS 
    Article 

    Google Scholar 
    Celdrán, D., Espinosa, E., Sánchez-Amat, A. & Marín, A. Effects of epibiotic bacteria on leaf growth and epiphytes of the seagrass Posidonia oceanica. Mar. Ecol. Prog. Ser. 456, 21–27 (2012).ADS 
    Article 

    Google Scholar 
    Brodersen, K. E., Koren, K., Revsbech, N. P. & Kühl, M. Strong leaf surface basification and CO2 limitation of seagrass induced by epiphytic biofilm microenvironments. Plant Cell Environ. 43, 174–187 (2020).CAS 
    Article 

    Google Scholar 
    Noisette, F., Depetris, A., Kühl, M. & Brodersen, K. E. Flow and epiphyte growth effects on the thermal, optical and chemical microenvironment in the leaf phyllosphere of seagrass (Zostera marina). J. R. Soc. Interface 17(171), 20200485 (2020).Article 

    Google Scholar 
    Costa, M. M. et al. Epiphytes modulate posidonia oceanica photosynthetic production, energetic balance, antioxidant mechanisms, and oxidative damage. Front. Mar. Sci. 2, 111 (2015).Article 

    Google Scholar 
    Guilini, K. et al. Response of Posidonia oceanica seagrass and its epibiont communities to ocean acidification. PLoS ONE 12(8), e0181531 (2017).Article 

    Google Scholar 
    Palacios, S. L. & Zimmerman, R. C. Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar. Ecol. Prog. Ser. 344, 1–13 (2007).ADS 
    Article 

    Google Scholar 
    Scartazza, A. et al. Carbon and nitrogen allocation strategy in Posidonia oceanica is altered by seawater acidification. Sci. Total Environ. 607, 954–964 (2017).ADS 
    Article 

    Google Scholar 
    Hansen, A. B., Pedersen, A. S., Kühl, M. & Brodersen, K. E. Temperature Effects on Leaf and Epiphyte Photosynthesis, Bicarbonate Use and Diel O 2 Budgets of the Seagrass Zostera marina L. Front. Mar. Sci. 9, (2022).Burnell, O. W., Russell, B. D., Irving, A. D. & Connell, S. D. Seagrass response to CO2 contingent on epiphytic algae: indirect effects can overwhelm direct effects. Oecologia 1, 871–882 (2014).ADS 
    Article 

    Google Scholar 
    Mabrouk, L., Hamza, A., Brahim, B. & Bradai, M.-N. Variability in the structure of epiphyte assemblages on leaves and rhizomes of Posidonia oceanica in relation to human disturbances in a seagrass meadow off Tunisia. Aquat. Bot. 108, 33–40 (2013).Article 

    Google Scholar 
    Garrard, S. L. et al. Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. J. Exp. Mar. Bio. Ecol. 461, 31–38 (2014).Article 

    Google Scholar 
    Touchette, B. W. & Burkholder, J. A. M. Review of nitrogen and phosphorus metabolism in seagrasses. J. Exp. Mar. Bio. Ecol. 250, 133–167 (2000).CAS 
    Article 

    Google Scholar 
    Borg, J. A., Rowden, A. A., Attrill, M. J., Schembri, P. J. & Jones, M. B. Wanted dead or alive: high diversity of macroinvertebrates associated with living and ‘dead’ Posidonia oceanica matte. Mar. Biol. 149, 667–677 (2006).Article 

    Google Scholar 
    Teixidó, N. et al. Functional biodiversity loss along natural CO 2 gradients. Nat. Commun. 9(1), 1–9 (2018).Article 

    Google Scholar  More

  • in

    Optimizing the Dryland Sheet Erosion equation in South China

    Feng, T. et al. Modeling soil erosion using a spatially distributed model in a karst catchment of northwest Guangxi, China. Earth Surf. Process. Landf. 39, 1005 (2015).
    Google Scholar 
    Bodoque, J. M. et al. Source of error and uncertainty in sheet erosion rates estimated from dendrogeomorphology. Earth Surf. Process. Landf. 40(9), 1146–1157 (2015).ADS 
    Article 

    Google Scholar 
    Larney, F. J. et al. Erosion–productivity–soil amendment relationships for wheat over 16 years. Soil Tillage Res. 103(1), 73–83 (2009).Article 

    Google Scholar 
    Xiao, H. et al. Response of soil detachment rate to the hydraulic parameters of concentrated flow on steep loessial slopes on the Loess Plateau of China. Hydrol. Process. 31(14), 2613–2621 (2017).ADS 
    Article 

    Google Scholar 
    Wei, W. et al. Effect of rainfall variation and landscape change on runoff and sediment yield from a loess hilly catchment in China. Environ. Earth Sci. 73(3), 1005–1016 (2015).Article 

    Google Scholar 
    Yu, F. A. et al. Effects of surface coal mining and land reclamation on soil properties: A review. Earth-Sci. Rev. 191, 12–25 (2019).Article 

    Google Scholar 
    Valmis, S., Dimoyiannis, D. & Danalatos, N. G. Assessing interrill erosion rate from soil aggregate instability index, rainfall intensity and slope angle on cultivated soils in central Greece. Soil Tillage Res. 80(1–2), 139–147 (2005).Article 

    Google Scholar 
    Qz, A. et al. Plot-based experimental study of raindrop detachment, interrill wash and erosion-limiting degree on a clayey loessal soil. J. Hydrol. 575, 1280–1287 (2019).Article 

    Google Scholar 
    Dongdong, W. et al. Sheet erosion rates and erosion control on steep rangelands in loess regions: Sheet erosion rates and erosion control on steep rangelands. Earth Surf. Process. Landf. 43, 146 (2018).
    Google Scholar 
    Mohammad, A. G. & Adam, M. A. The impact of vegetative cover type on runoff and soil erosion under different land uses. Catena 81(2), 97–103 (2010).Article 

    Google Scholar 
    Shin, J. Y. et al. Spatial and temporal variations in rainfall erosivity and erosivity density in South Korea. Catena. 176, 125–144 (2019).Article 

    Google Scholar 
    Wang, D. et al. Characterisation of soil erosion and overland flow on vegetation-growing slopes in fragile ecological regions: A review. J. Environ. Manag. 285, 1400 (2021).
    Google Scholar 
    Li, Z. W. et al. Rill erodibility as influenced by soil and land use in a small watershed of the Loess Plateau, China. Biosyst. Eng. 129, 248–257 (2015).Article 

    Google Scholar 
    Yu, L. et al. Hydrological responses and soil erosion potential of abandoned cropland in the loess plateau, China. Geomorphology 138(1), 404–414 (2012).ADS 
    Article 

    Google Scholar 
    Nearing, M. A., Bradford, J. M. & Parker, S. C. Soil detachment by shallow flow at low slopes. Soil Sci. Soc. Am. J. 55(2), 351–357 (1991).Article 

    Google Scholar 
    Prosser, I. P. & Rustomji, P. Sediment transport capacity relations for overland flow. Prog. Phys. Geogr. 24, 179–193 (2000).Article 

    Google Scholar 
    Yang, C. T. Minimum unit stream power and fluvial hydraulics. J. Hydraul. Div. 102(7), 769–784 (1976).
    Google Scholar 
    Zhao, Z. X. & He, J. J. Hydraulics 2nd edn, 193–198 (Springer, 2010).
    Google Scholar 
    Zhang, M. et al. The response of soil microbial communities to soil erodibility depends on the plant and soil properties in semiarid regions. Land Degrad. Dev. 7, 14005 (2021).
    Google Scholar 
    Zhang, K. L. et al. Soil erodibility and its estimation for agricultural soils in China. Acta Pedol. Sin. 72(6), 1002–1011 (2008).
    Google Scholar 
    Long, S. et al. Soil surface roughness change and its effect on runoff and erosion on the Loess Plateau of China. J. Arid Land. 6(4), 400–409 (2014).Article 

    Google Scholar 
    Zhang, Y. W. et al. Changes in soil water holding capacity and water availability following vegetation restoration on the Chinese Loess Plateau. Sci. Rep. 11(1), 1000 (2021).Article 

    Google Scholar 
    Liu, J. et al. Sediment transport capacity and its response to hydraulic parameters in experimental rill flow on steep slope. J. Soil Water Conserv. 70, 36–44 (2018).
    Google Scholar 
    Vargas-Luna, A., Crosato, A. & Uijttewaal, W. S. J. Effects of vegetation on flow and sediment transport: comparative analyses and validation of predicting models. Earth Surf. Process. Landf. 40(2), 157–176 (2015).ADS 
    Article 

    Google Scholar 
    Wang, J. G. et al. Particle size and shape variation of Ultisol aggregates affected by abrasion under different transport distances in overland flow. Catena 123, 153–162 (2014).CAS 
    Article 

    Google Scholar 
    Wang, D. et al. Modeling soil detachment capacity by rill flow using hydraulic parameters. J. Hydrol. 535, 473–479 (2016).ADS 
    Article 

    Google Scholar 
    Zhang, B. J. et al. Soil resistance to flowing water erosion of seven typical plant communities on steep gully slopes on the Loess Plateau of China. Catena. 173, 375–383 (2019).Article 

    Google Scholar 
    Maïga-Yaleu, S. B. et al. Impact of sheet erosion mechanisms on organic carbon losses from crusted soils in the Sahel. Catena 126, 60–67 (2015).Article 

    Google Scholar 
    Mo, M. et al. Water and sediment runoff and soil moisture response to grass cover in sloping citrus land, Southern China. Soil Water Res. 14(1), 1004 (2018).
    Google Scholar 
    Jin, F. et al. Effects of vegetation and climate on the changes of soil erosion in the Loess Plateau of China. Sci. Total Enviro. 773, 10078 (2021).Article 

    Google Scholar 
    Yu, M. et al. Impact of land-use changes on soil hydraulic properties of Calcaric Regosols on the Loess Plateau, NW China. J. Plant Nutr. Soil Sci. 178(3), 486–498 (2018).Article 

    Google Scholar 
    Liu, W. Isotopic indicators of carbon and nitrogen cycles in river catchments during soil erosion in the arid loess plateau of china. Chem. Geol. 296–297, 66–72 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    Cheng, M. & Shaoshan, A. N. Response of soil nitrogen, phosphorous and organic matter to vegetation succession on the Loess Plateau of China. J. Arid Land. 7(2), 216–223 (2015).Article 

    Google Scholar 
    Zhang, G. H. et al. Influence of vegetation parameters on runoff and sediment characteristics in patterned Artemisia capillaris plots. J. Arid Land. 2, 1440 (2014).
    Google Scholar 
    Hao, H. X. et al. Vegetation restoration and fine roots promote soil infiltrability in heavy-textured soils. Soil Tillage Res. 198, 104542 (2020).Article 

    Google Scholar 
    Chen, Y. et al. Soil enzyme activities of typical plant communities after vegetation restoration on the Loess Plateau, China. China Appl. Soil Ecol. 170, 104292 (2020).Article 

    Google Scholar 
    Mga, B. et al. Revegetation induced change in soil erodibility as influenced by slope situation on the Loess Plateau. Sci. Total Environ. 2, 158 (2021).
    Google Scholar 
    Ma, L. et al. Effects of earthworm (Metaphire guillelmi) density on soil macropore and soil water content in typical Anthrosol soil. Agric. Ecosyst. Environ. 311(5), 107338 (2021).Article 

    Google Scholar 
    Chen, Y. et al. Soil enzyme activities of typical plant communities after vegetation restoration on the Loess Plateau, China. China Appl. Soil Ecol. 170, 104292 (2020).Article 

    Google Scholar 
    Xu, W. et al. Strengthening protected areas for biodiversity and ecosystem services in China. Proc. Natl. Acad. Sci. USA 114(7), 1601 (2017).CAS 
    Article 

    Google Scholar 
    Ran, Q., Wang, F. & Gao, J. The effect of storm movement on infiltration, runoff and soil erosion in a semi-arid catchment. Hydrol. Process. 6, 7600 (2020).
    Google Scholar  More

  • in

    Oogenesis and lipid metabolism in the deep-sea sponge Phakellia ventilabrum (Linnaeus, 1767)

    Bergé, J.-P. & Barnathan, G. Fatty acids from lipids of marine organisms: Molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Adv. Biochem. Eng. Biotechnol. 96, 49–125 (2005).
    Google Scholar 
    Parzanini, C., Parrish, C., Hamel, J. & Mercier, A. Functional diversity and nutritional content in a deep-sea faunal assemblage through total lipid, lipid class, and fatty acid analyses. PLoS ONE 13, e0207395 (2018).Article 

    Google Scholar 
    Parrish, C. C. Lipids in marine ecosystems. ISRN Oceanogr. 2013, 1–16 (2013).Article 

    Google Scholar 
    Parrish, C. et al. Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In Marine Chemistry. The Handbook of Environmental Chemistry (Vol. 5 Series: Water Pollution) Vol. 5 (ed. Wangersky, P. J.) (Springer, 2000).
    Google Scholar 
    Laender, F. D., Oevelen, D. V., Frantzen, S., Middelburg, J. J. & Soetaert, K. Seasonal PCB bioaccumulation in an arctic marine ecosystem: a model analysis incorporating lipid dynamics, food-web productivity and migration. Environ. Sci. Technol. 44, 356–361 (2010).Article 

    Google Scholar 
    Bianchi, T. & Canuel, E. Chemical Biomarkers in Aquatic Ecosystems (Princeton University Press, 2011).Book 

    Google Scholar 
    Signa, G. et al. Lipid and fatty acid biomarkers as proxies for environmental contamination in caged mussels Mytilus galloprovincialis. Ecol. Indic. 57, 384–394 (2015).CAS 
    Article 

    Google Scholar 
    Brett, M., Mueller-Navarra, D. & Persson, J. Crustacean zooplankton fatty acid composition. In Lipids in Aquatic Ecosystems (eds Kainz, M. et al.) 115–146 (Springer, 2009).Chapter 

    Google Scholar 
    Martin-Creuzburg, D. & Elert, E. Ecological significance of sterols in aquatic food webs. In Lipids in Aquatic Ecosystems (eds Kainz, M. et al.) 43–64 (Springer, 2009).Chapter 

    Google Scholar 
    Parrish, C. Essential fatty acids in aquatic food webs. In Lipids in Aquatic Ecosystem (eds Kainz, M. et al.) 309–326 (Springer, 2009).Chapter 

    Google Scholar 
    Maier, S. R., Bannister, R. J., van Oevelen, D. & Kutti, T. Seasonal controls on the diet, metabolic activity, tissue reserves and growth of the cold-water coral Lophelia pertusa. Coral Reefs 39, 173–187 (2020).Article 

    Google Scholar 
    Phleger, C. F. Buoyancy in marine fishes: Direct and indirect role of lipids. Am. Zool. 38, 321–330 (1998).CAS 
    Article 

    Google Scholar 
    Pond, D. W. & Tarling, G. A. Phase transitions of wax esters adjust buoyancy in diapausing Calanoides acutus. Limnol. Oceanogr. 56, 1310–1318 (2011).CAS 
    Article 

    Google Scholar 
    Giese, A. C. Lipids in the economy of marine invertebrates. Physiol. Rev. 46, 244–298 (1966).CAS 
    Article 

    Google Scholar 
    Joseph, J. D. Distribution and composition of lipids in marine invertebrates. In Marine Biogenic Lipids, Fats and Oils (ed. Ackman, R. G.) 49–143 (CRC Press, 1989).
    Google Scholar 
    Lee, R. F. Lipoproteins from the hemolymph and ovaries of marine invertebrates. In Advances in Comparative and Environmental Physiology (eds Houlihan, D. F. et al.) 187–207 (Springer, 1991).Chapter 

    Google Scholar 
    Kattner, G. & Hagen, W. Lipid metabolism of the Antarctic euphausiid Euphausia crystallorophias and its ecological implications. Mar. Ecol. Prog. Ser. 170, 203–213 (1998).CAS 
    Article 

    Google Scholar 
    Heras, H., Pollero, R. J., Gonzalez-Baró, M. R. & Pollero, R. J. Lipid and fatty acid composition and energy partitioning during embryo development in the shrimp Macrobrachium borellii. Lipids 35, 645–651 (2000).CAS 
    Article 

    Google Scholar 
    Viladrich, N. et al. Variation in lipid and free fatty acid content during spawning in two temperate octocorals with different reproductive strategies: surface versus internal brooder. Coral Reefs 35, 1033–1045 (2016).Article 

    Google Scholar 
    Hansen, M., Flatt, T. & Aguilaniu, H. Reproduction, fat metabolism, and lifespan—What is the connection?. Cell Metab. 17, 10–19 (2013).CAS 
    Article 

    Google Scholar 
    Strathmann, R. R. Egg size, larval development, and juvenile size in benthic marine invertebrates. Am. Nat. 111, 373–376 (1977).Article 

    Google Scholar 
    Pechenik, J. Delayed metamorphosis by larvae of benthic marine-invertebrates—Does it occur? Is there a price to pay?. Ophelia 32, 63–94 (1990).Article 

    Google Scholar 
    Harms, J. Larval development and delayed metamorphosis in the hermit crab Clibanarius erythropus (Latreille) (Crustacea, Diogenidae). J. Exp. Mar. Bio. Ecol. 156, 151–160 (1992).Article 

    Google Scholar 
    Harii, S., Kayanne, H., Takigawa, H. T., Hayashibara, T. H. & Yamamoto, M. Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar. Biol. 141, 39–46 (2002).Article 

    Google Scholar 
    Doughty, P. & Shine, R. Detecting life history trade-offs: measuring energy stores in “capital” breeders reveals costs of reproduction. Oecologia 110, 508–513 (1997).Article 

    Google Scholar 
    Coma, R., Ribes, M., Gili, J.-M. & Zabala, M. An energetic approach to the study of life-history traits of two modular colonial benthic invertebrates. Mar. Ecol. Prog. Ser. 162, 89–103 (1998).Article 

    Google Scholar 
    Rossi, S. et al. Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavata (Anthozoa, Octocorallia): Evidence for summer–autumn feeding constraints. Mar. Biol. 149, 643–651 (2006).CAS 
    Article 

    Google Scholar 
    Kattner, G., Graeve, M. & Hagen, W. Ontogenetic and seasonal changes in lipid and fatty acid/alcohol compositions of the dominant Antarctic copepods Calanus propinquus, Calanoides acutus and Rhincalanus gigas. Mar. Biol. 644, 18119 (1994).
    Google Scholar 
    Lee, R. F., Hagen, W. & Kattner, G. Lipid storage in marine zooplankton. Mar. Ecol. Prog. Ser. 307, 273–306 (2006).CAS 
    Article 

    Google Scholar 
    Mourente, G., Medina, A., González, S. & Rodríguez, A. Variations in lipid content and nutritional status during larval development of the marine shrimp Penaeus kerathurus. Aquaculture 130, 187–199 (1995).CAS 
    Article 

    Google Scholar 
    Marshall, C. T., Yaragina, N. A., Lambert, Y. & Kjesbu, O. S. Total lipid energy as a proxy for total egg production by fish stocks. Nature 402, 288–290 (1999).CAS 
    Article 

    Google Scholar 
    Marshall, C. T., Yaragina, N. A., Ådlandsvik, B. & Dolgov, A. V. Reconstructing the stock-recruit relationship for Northeast Arctic cod using a bioenergetic index of reproductive potential. Can. J. Fish. Aquat. Sci. 57, 2433–2442 (2000).Article 

    Google Scholar 
    Dalsgaard, J., St. John, M., Kattner, G., Müller-Navarra, D. & Hagen, W. B. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46, 225–340 (2003).Article 

    Google Scholar 
    Bergquist, P. R., Lawson, M. P., Lavis, A. & Cambie, R. C. Fatty acid composition and the classification of the Porifera. Biochem. Syst. Ecol. 12, 63–84 (1984).CAS 
    Article 

    Google Scholar 
    Djerassi, C. & Lam, W. K. Sponge phospholipids. Acc. Chem. Res. 24, 69–75 (1991).CAS 
    Article 

    Google Scholar 
    Thiel, V. et al. A chemical view of the most ancient metazoa – Biomarker chemotaxonomy of hexactinellid sponges. Naturwissenschaften 89, 60–66 (2002).CAS 
    Article 

    Google Scholar 
    Velosaotsy, N. et al. Phospholipid distribution and phospholipid fatty acids in four Saudi red sea sponges. Boll. Mus. Ist. Biol. Univ. Genova 68, 639–645 (2004).
    Google Scholar 
    Rod’kina, S. A. Fatty acids and other lipids of marine sponges. Russ. J. Mar. Biol. 31, S49–S60 (2005).Article 

    Google Scholar 
    Blumenberg, M. & Michaelis, W. High occurrences of brominated lipid fatty acids in boreal sponges of the order Halichondrida. Mar. Biol. 150, 1153–1160 (2007).CAS 
    Article 

    Google Scholar 
    Genin, E. et al. New trends in phospholipid class composition of marine sponges. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 150, 427–431 (2008).Article 

    Google Scholar 
    Müller, W. et al. Role of the aggregation factor in the regulation of phosphoinositide metabolism in sponges. Possible consequences on calcium efflux and on mitogenesis. J. Biol. Chem. 262, 9850–9858 (1987).Article 

    Google Scholar 
    Weissmann, G., Riesen, W., Davidson, S. & Waite, M. Stimulus-response coupling in marine sponge cell aggregation: Lipid metabolism and the function of exogenously added arachidonic and docosahexaenoic acids. Biochim. Biophys. Acta 960, 351–364 (1988).CAS 
    Article 

    Google Scholar 
    Zivanovic, A., Pastro, N. J., Fromont, J., Thomson, M. & Skropeta, D. Kinase inhibitory, haemolytic and cytotoxic activity of three deep-water sponges from North Western Australia and their fatty acid composition. Nat. Prod. Commun. 6, 1921–1924 (2011).CAS 

    Google Scholar 
    Shaaban, M., Abd-Alla, H. I., Hassan, A. Z., Aly, H. F. & Ghani, M. A. Chemical characterization, antioxidant and inhibitory effects of some marine sponges against carbohydrate metabolizing enzymes. Org. Med. Chem. Lett. 2, 30 (2012).Article 

    Google Scholar 
    Botić, T. et al. Fatty acid composition and antioxidant activity of Antarctic marine sponges of the genus Latrunculia. Polar Biol. 38, 1605–1612 (2015).Article 

    Google Scholar 
    Bennett, H., Bell, J. J., Davy, S. K., Webster, N. S. & Francis, D. S. Elucidating the sponge stress response; lipids and fatty acids can facilitate survival under future climate scenarios. Glob. Chang. Biol. 24, 3130–3144 (2018).Article 

    Google Scholar 
    Carballeira, N. M. New advances in fatty acids as antimalarial, antimycobacterial and antifungal agents. Prog. Lipid Res. 47, 50–61 (2008).CAS 
    Article 

    Google Scholar 
    Kikuchi, H. et al. Marine natural products. X. Pharmacologically active glycolipids from the Okinawan marine sponge Phyllospongia foliascens (Pallas). Chem. Pharm. Bull. (Tokyo) 30, 3544–3547 (1982).CAS 
    Article 

    Google Scholar 
    Natori, T., Morita, M., Akimoto, K. & Koezuka, Y. Agelasphins, novel antitumor and immunostimulatory cerebrosides from the marine sponge Agelas mauritianus. Tetrahedron 50, 2771–2784 (1994).CAS 
    Article 

    Google Scholar 
    Costantino, V., Fattorusso, E., Mangoni, A., Di Rosa, M. & Ianaro, A. Glycolipids from Sponges. 6. Plakoside A and B, two unique prenylated glycosphingolipids with Immunosuppressive activity from the marine sponge Plakortis simplex. J. Am. Chem. Soc. 119, 12465–12470 (1997).CAS 
    Article 

    Google Scholar 
    Costantino, V., Fattorusso, E., Imperatore, C. & Mangoni, A. Glycolipids from sponges. 11. Isocrasserides, novel glycolipids with a five-membered cyclitol widely distributed in marine sponges. J. Nat. Prod. 65, 883–886 (2002).CAS 
    Article 

    Google Scholar 
    Maldonado, M. & Riesgo, A. Reproduction in Porifera: a synoptic overview. Treballs la Soc. Catalana Biol. 59, 29–49 (2008).
    Google Scholar 
    Sciscioli, M., Lepore, E., Scalera-Liaci, L. & Gherardi, M. Indagine ultrastrutturale sugli ovociti di Erylus discophorus (Schmidt) (Porifera, Tetractinellida). Oebalia 15, 939–941 (1989).
    Google Scholar 
    Sciscioli, M., Liaci, L. S., Lepore, E., Gherardi, M. & Simpson, T. L. Ultrastructural study of the mature egg of the marine sponge Stelletta grubii (porifera demospongiae). Mol. Reprod. Dev. 28, 346–350 (1991).CAS 
    Article 

    Google Scholar 
    Riesgo, A. et al. Some like it fat: comparative ultrastructure of the embryo in two demosponges of the genus Mycale (order Poecilosclerida) from Antarctica and the Caribbean. PLoS ONE 10, e0118805 (2015).Article 

    Google Scholar 
    Watanabe, Y. The development of two species of Tetilla (Demosponge). NSR. O. U. 29, 71–106 (1978).
    Google Scholar 
    Gaino, E. & Sarà, M. An ultrastructural comparative study of the eggs of two species of Tethya (Porifera, Demospongiae). Invertebr. Reprod. Dev. 26, 99–106 (1994).Article 

    Google Scholar 
    Maldonado, M. & Riesgo, A. Gametogenesis, embryogenesis, and larval features of the oviparous sponge Petrosia ficiformis (Haplosclerida, Demospongiae). Mar. Biol. 156, 2181–2197 (2009).Article 

    Google Scholar 
    Lanna, E. & Klautau, M. Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129, 249–261 (2010).Article 

    Google Scholar 
    Koutsouveli, V. et al. Insights into the reproduction of some Antarctic dendroceratid, poecilosclerid, and haplosclerid demosponges. PLoS ONE 13, 1–24 (2018).Article 

    Google Scholar 
    Fell, P. E. The involvement of nurse cells in oogenesis and embryonic development in the marine sponge, Haliclona ecbasis. J. Morphol. 127, 133–149 (1969).Article 

    Google Scholar 
    Simpson, T. The Cell Biology of Sponges (Springer, 1984).Book 

    Google Scholar 
    Bellairs, R. The structure of the yolk of the hen’s egg as studied by electron microscopy : i. The yolk of the unincubated egg. J. Biophys. Biochem. Cytol. 11, 207–225 (1961).CAS 
    Article 

    Google Scholar 
    Ereskovsky, A. The Comparative Embryology of Sponges (Springer, 2010).Book 

    Google Scholar 
    Sarà, A., Cerrano, C. & Sarà, M. Viviparous development in the Antarctic sponge Stylocordyla borealis Loven, 1868. Polar Biol. 25, 425–431 (2002).Article 

    Google Scholar 
    Busch, K. et al. Chloroflexi dominate the deep-sea golf ball sponges Craniella zetlandica and Craniella infrequens throughout different life stages. Front. Mar. Sci. 7, 674 (2020).Article 

    Google Scholar 
    Koopmans, M. et al. Seasonal variation of fatty acids and stable carbon isotopes in sponges as indicators for nutrition: Biomarkers in sponges identified. Mar. Biotechnol. 17, 43–54 (2015).CAS 
    Article 

    Google Scholar 
    Lüskow, F. et al. Seasonality in lipid content of the demosponges Halichondria panicea and H. bowerbanki at two study sites in temperate Danish waters. Front. Mar. Sci. 6, 1–7 (2019).Article 

    Google Scholar 
    Reiswig, H. Population dynamics of three Jamaican demospongiae. Bull. Mar. Sci. 23, 191–226 (1973).
    Google Scholar 
    Elvin, D. W. Seasonal growth and reproduction of an intertidal sponge, Haliclona permollis (Bowerbank). Univ. Chicago Press 151, 108–125 (1976).
    Google Scholar 
    Elvin, D. W. The relationship of seasonal changes in the biochemical components to the reproductive behavior of the intertidal sponge, Haliclona permollis. Biol Bull. 156, 47–61 (1979).CAS 
    Article 

    Google Scholar 
    Barthel, D. On the ecophysiology of the sponge Halichondria panicea in Kiel Bight. I. Substrate specificity, growth and reproduction. Mar. Ecol. Prog. Ser. 32, 291–298 (1986).Article 

    Google Scholar 
    Ivanisevic, J., Pérez, T., Ereskovsky, A. V., Barnathan, G. & Thomas, O. P. Lysophospholipids in the Mediterranean sponge Oscarella tuberculata: Seasonal variability and putative biological role. J. Chem. Ecol. 37, 537 (2011).CAS 
    Article 

    Google Scholar 
    Klitgaard, A. B. The fauna associated with outer shelf and upper slope sponges (Porifera, demospongiae) at the Faroe islands, North-eastern Atlantic. Sarsia 80, 1–22 (1995).Article 

    Google Scholar 
    Klitgaard, A. B. & Tendal, O. Distribution and species composition of mass occurrences of large-sized sponges in the northeast Atlantic. Prog. Oceanogr. 61, 57–98 (2004).Article 

    Google Scholar 
    Kutti, T., Bannister, R. J. & Fosså, J. H. Community structure and ecological function of deep-water sponge grounds in the Traenadypet MPA—Northern Norwegian continental shelf. Cont. Shelf Res. 69, 21–30 (2013).Article 

    Google Scholar 
    Pile, A. & Young, C. The natural diet of a hexactinellid sponge: Benthic–pelagic coupling in a deep-sea microbial food web. Deep Sea Res. Part I Oceanogr. Res. Pap. 53, 1148–1156 (2006).Article 

    Google Scholar 
    Yahel, G., Whitney, F., Reiswig, H. M., Eerkes-Medrano, D. I. & Leys, S. P. In situ feeding and metabolism of glass sponges (Hexactinellida, Porifera) studied in a deep temperate fjord with a remotely operated submersible. Limnol. Oceanogr. 52, 428–440 (2007).CAS 
    Article 

    Google Scholar 
    Hoffmann, F. et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11, 2228–2243 (2009).CAS 
    Article 

    Google Scholar 
    Cathalot, C. et al. Cold-water coral reefs and adjacent sponge grounds: hotspots of benthic respiration and organic carbon cycling in the deep sea. Front. Mar. Sci. 2, 1–12 (2015).Article 

    Google Scholar 
    Kahn, A., Yahel, G., Chu, J., Tunnicliffe, V. & Leys, S. Benthic grazing and carbon sequestration by deep-water glass sponge reefs. Limnol. Oceanogr. 60, 78–88 (2015).Article 

    Google Scholar 
    Rooks, C. et al. Deep-sea sponge grounds as nutrient sinks: denitrification is common in boreo-Arctic sponges. Biogeosciences 17, 1231–1245 (2020).CAS 
    Article 

    Google Scholar 
    Koutsouveli, V., Cárdenas, P., Conejero, M., Rapp, H. T. & Riesgo, A. Reproductive biology of Geodia species (Porifera, Tetractinellida) from Boreo-Arctic North-Atlantic Deep-Sea Sponge Grounds. Front. Mar. Sci. 7, 1–22 (2020).Article 

    Google Scholar 
    Reynolds, E. S. The use of lead citrate at high PH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).CAS 
    Article 

    Google Scholar 
    Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
    Article 

    Google Scholar 
    Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).CAS 
    Article 

    Google Scholar 
    Balgoma, D. et al. Anabolic androgenic steroids exert a selective remodeling of the plasma lipidome that mirrors the decrease of the de novo lipogenesis in the liver. Metabolomics 16, 12 (2020).CAS 
    Article 

    Google Scholar 
    Kolmert, J. et al. Prominent release of lipoxygenase generated mediators in a murine house dust mite-induced asthma model. Prostaglandins Other Lipid Mediat. 137, 20–29 (2018).CAS 
    Article 

    Google Scholar 
    Balgoma, D. et al. Linoleic acid-derived lipid mediators increase in a female-dominated subphenotype of COPD. Eur. Respir. J. 47, 1645–1656 (2016).CAS 
    Article 

    Google Scholar 
    Smith, C. A., Want, E. J., O’Maille, G., Abagyan, R. & Siuzdak, G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal. Chem. 78, 779–787 (2006).CAS 
    Article 

    Google Scholar 
    Tautenhahn, R., Böttcher, C. & Neumann, S. Highly sensitive feature detection for high resolution LC/MS. BMC Bioinform. 9, 504 (2008).Article 

    Google Scholar 
    Fahy, E., Sud, M., Cotter, D. & Subramaniam, S. LIPID MAPS online tools for lipid research. Nucleic Acids Res. 35, W606–W612 (2007).Article 

    Google Scholar 
    Böcker, S., Letzel, M. C., Lipták, Z. & Pervukhin, A. SIRIUS: decomposing isotope patterns for metabolite identification. Bioinformatics 25, 218–224 (2008).Article 

    Google Scholar 
    Koutsouveli, V. et al. The molecular machinery of gametogenesis in Geodia demosponges (Porifera): Evolutionary origins of a conserved toolkit across animals. Mol. Biol. Evol. 37, 3485–3506 (2020).CAS 
    Article 

    Google Scholar 
    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
    Article 

    Google Scholar 
    Grabherr, M. G. et al. Trinity: reconstructing a full-length transcriptome without a genome assembly from RNA-Seq data. Nat. Biotechnol. 29, 644–652 (2011).CAS 
    Article 

    Google Scholar 
    Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).Article 

    Google Scholar 
    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).CAS 
    Article 

    Google Scholar 
    Li, B. & Dewey, C. N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12, 323 (2011).CAS 
    Article 

    Google Scholar 
    Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2009).Article 

    Google Scholar 
    McCarthy, D. J., Chen, Y. & Smyth, G. K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288–4297 (2012).CAS 
    Article 

    Google Scholar 
    Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997).CAS 
    Article 

    Google Scholar 
    Boeckmann, B. et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31, 365–370 (2003).CAS 
    Article 

    Google Scholar 
    Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59 (2014).Article 

    Google Scholar 
    Conesa, A. et al. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).CAS 
    Article 

    Google Scholar 
    Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).CAS 
    Article 

    Google Scholar 
    Busch, K. et al. Population connectivity of fan-shaped sponge holobionts in the deep Cantabrian Sea. Deep Sea Res. Part I Oceanogr. Res. Pap. 167, 103427 (2020).Article 

    Google Scholar 
    Southwood, T. R. Habitat, the templet for ecological strategies. J. Anim. Ecol. 46, 336–365 (1977).Article 

    Google Scholar 
    Clarke, A. A reappraisal of the concept of metabolic cold adaptation in polar marine invertebrates. Biol. J. Linn. Soc. 14, 77–92 (1980).Article 

    Google Scholar 
    Witte, U. Seasonal reproduction in deep-sea sponges—Triggered by vertical particle flux?. Mar. Biol. 124, 571–581 (1996).Article 

    Google Scholar 
    Spetland, F., Rapp, H. T., Hoffmann, F. & Tendal, O. S. Sexual reproduction of Geodia barretti Bowerbank, 1858 (Porifera, Astrophorida) in two Scandinavian fjords. In Porifera Research: Biodiversity, Innovation, Sustainability Vol. 1858 (eds Custódio, M. et al.) 613–620 (Série Livros. Museu Nacional, 2007).
    Google Scholar 
    Wassmann, P. Dynamics of primary production and sedimentation in shallow fjords and polls of western Norway. Oceanogr. Mar. Biol. Annu. Rev. 29, 87–154 (1991).
    Google Scholar 
    Wassmann, P., Svendsen, H., Keck, A. & Reigstad, M. Selected aspects of the physical oceanography and particle fluxes in fjords of northern Norway. J. Mar. Syst. 8, 53–71 (1996).Article 

    Google Scholar 
    Bamstedt, U. Life cycle, seasonal vertical distribution and feeding of Calanus finmarchicus in Skagerrak coastal water. Mar. Biol. 137, 279–289 (2000).Article 

    Google Scholar 
    Eckelbarger, K. J. & Watling, L. Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invertebr. Biol. 114, 256–269 (1995).Article 

    Google Scholar 
    Riesgo, A. & Maldonado, M. Ultrastructure of oogenesis of two oviparous demosponges: Axinella damicornis and Raspaciona aculeata (Porifera). Tissue Cell 41, 51–65 (2009).Article 

    Google Scholar 
    Whiteley, N. M., Taylor, E. W. & el Haj, A. J. A comparison of the metabolic cost of protein synthesis in stenothermal and eurythermal isopod crustaceans. Am. J. Physiol. 271, R1295–R1303 (1996).CAS 
    Article 

    Google Scholar 
    Pace, D. A. & Manahan, D. T. Cost of protein synthesis and energy allocation during development of Antarctic sea urchin embryos and larvae. Biol. Bull. 212, 115–129 (2007).CAS 
    Article 

    Google Scholar 
    Sciscioli, M., Lepore, E., Gherardi, M. & Liaci, L. S. Transfer of symbiotic bacteria in the mature oocyte of Geodia cydonium (Porifera, Demosponsgiae): An ultrastructural study. Cah. Biol. Mar. 35, 471–478 (1994).
    Google Scholar 
    McWilliams, S. R., Guglielmo, C., Pierce, B. & Klaassen, M. Flying, fasting, and feeding in birds during migration: A nutritional and physiological ecology perspective. J. Avian Biol. 35, 377–393 (2004).Article 

    Google Scholar 
    Derickson, W. K. Lipid storage and utilization in reptiles. Am. Zool. 16, 711–723 (1976).CAS 
    Article 

    Google Scholar 
    Fraser, A. J. Triacylglycerol content as a condition index for fish, bivalve, and crustacean larvae. Can. J. Fish. Aquat. Sci. 46, 1868–1873 (1989).CAS 
    Article 

    Google Scholar 
    Bonnet, X., Naulleau, G. & Mauget, R. The influence of body condition on 17-beta estradiol levels in relation to vitellogenesis in female Vipera aspis (Reptilia, Viperidae). Gen. Comp. Endocrinol. 93, 424–437 (1994).CAS 
    Article 

    Google Scholar 
    Duggan, A. et al. Seasonal variation in plasma lipids, lipoproteins, apolipoprotein A-I and vitellogenin in the freshwater turtle, Chrysemys picta. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 130, 253–269 (2001).CAS 
    Article 

    Google Scholar 
    Lance, V. A., Place, A. R., Grumbles, J. S. & Rostal, D. C. Variation in plasma lipids during the reproductive cycle of male and female desert tortoises, Gopherus agassizii. J. Exp. Zool. 293, 703–711 (2002).CAS 
    Article 

    Google Scholar 
    Kawazu, I. et al. Signals of vitellogenesis and estrus in female hawksbill turtles. Zoolog. Sci. 32, 114–118 (2015).Article 

    Google Scholar 
    Teshima, S. & Kanazawa, A. Variation in lipid compositions during the ovarian maturation of the prawn. Nippon Suisan Gakkaishi 49, 957–962 (1983).CAS 
    Article 

    Google Scholar 
    Clarke, A., Brown, J. H. & Holmes, L. J. The biochemical composition of eggs from Macrobrachium rosenbergii in relation to embryonic development. Comp. Biochem. Physiol. Part B Comp. Biochem. 96, 505–511 (1990).Article 

    Google Scholar 
    Allen, W. Amino acid and fatty acid composition of tissues of the dungeness crab (Cancer magister). J. Fish. Res. Board Canada 28, 1191–1195 (1971).CAS 
    Article 

    Google Scholar 
    Rosa, R. & Nunes, M. L. Tissue biochemical composition in relation to the reproductive cycle of deep-sea decapod Aristeus antennatus in the Portuguese south coast. J. Mar. Biol. Assoc. U. K. 83, 963–970 (2003).CAS 
    Article 

    Google Scholar 
    Balgoma, D., Pettersson, C. & Hedeland, M. Common fatty markers in diseases with dysregulated lipogenesis. Trends Endocrinol. Metab. 30, 283–285 (2019).CAS 
    Article 

    Google Scholar 
    Kent, C. Eukaryotic phospholipid biosynthesis. Annu. Rev. Biochem. 64, 315–343 (1995).CAS 
    Article 

    Google Scholar 
    Coleman, R. A. & Lee, D. P. Enzymes of triacylglycerol synthesis and their regulation. Prog. Lipid Res. 43, 134–176 (2004).CAS 
    Article 

    Google Scholar 
    Bell, R. M. & Coleman, R. A. Enzymes of glycerolipid synthesis in eukaryotes. Annu. Rev. Biochem. 49, 459–487 (1980).CAS 
    Article 

    Google Scholar 
    Mathews, C., van Holde, K., Appling, D. & Anthony-Cahill, S. Biochemistry (Pearson, 2019).
    Google Scholar 
    Gavaud, J. Histochemical identification of ovarian lipids during vitellogenesis in the lizard Lacerta vivipara. Can. J. Zool. 69, 1389–1392 (1991).Article 

    Google Scholar 
    Chapman, M. J. Animal lipoproteins: Chemistry, structure, and comparative aspects. J. Lipid Res. 21, 789–853 (1980).CAS 
    Article 

    Google Scholar 
    Lebouvier, M., Miramón-Puértolas, P. & Steinmetz, P.R. Evolutionary conserved aspects of animal nutrient uptake and transport in sea anemone vitellogenesis. bioRxiv (2022).Dolphin, P. J., Ansari, A. Q., Lazier, C. B., Munday, K. A. & Akhtar, M. Studies on the induction and biosynthesis of vitellogenin, an oestrogen-induced glycolipophosphoprotein. Biochem. J. 124, 751–758 (1971).CAS 
    Article 

    Google Scholar 
    Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G. & Leys, S. P. The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol. Biol. Evol. 31, 1102–1120 (2014).CAS 
    Article 

    Google Scholar 
    Wanders, R. J. A. Peroxisomes, lipid metabolism, and peroxisomal disorders. Mol. Genet. Metab. 83, 16–27 (2004).CAS 
    Article 

    Google Scholar 
    Wanders, R. J. A., Waterham, H. R. & Ferdinandusse, S. Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum. Front. Cell Dev. Biol. 3, 83 (2016).Article 

    Google Scholar 
    Talley, J. & Mohiuddin, S. Biochemstry, Fatty Acid Oxidation (StatPearls, 2020).
    Google Scholar 
    Reiswig, H. M. Particle feeding in natural populations of three marine demosponges. Biol. Bull. 141, 568–591 (1971).Article 

    Google Scholar 
    Sugimoto, Y., Inazumi, T. & Tsuchiya, S. Roles of prostaglandin receptors in female reproduction. J. Biochem. 157, 73–80 (2015).CAS 
    Article 

    Google Scholar 
    Niringiyumukiza, J. D., Cai, H. & Xiang, W. Prostaglandin E2 involvement in mammalian female fertility: ovulation, fertilization, embryo development and early implantation. Reprod. Biol. Endocrinol. 16, 43 (2018).Article 

    Google Scholar 
    Kaczynski, P., Baryla, M., Goryszewska, E., Bauersachs, S. & Waclawik, A. Prostaglandin F2α promotes embryo implantation and development in the pig. Reproduction 156, 405–419 (2018).CAS 

    Google Scholar 
    De Petrocellis, L. & Di Marzo, V. Aquatic invertebrates open up new perspectives in eicosanoid research: Biosynthesis and bioactivity. Prostaglandins Leukot. Essent. Fat. Acids 51, 215–229 (1994).Article 

    Google Scholar 
    Destephano, D. B. & Brady, U. E. Prostaglandin and prostaglandin synthetase in the cricket, Acheta domesticus. J. Insect Physiol. 23, 905–911 (1977).CAS 
    Article 

    Google Scholar 
    Rich, A. M. et al. Calcium dependent aggregation of marine sponge cells is provoked by leukotriene B4 and inhibited by inhibitors of arachidonic acid oxidation. Biochem. Biophys. Res. Commun. 121, 863–870 (1984).CAS 
    Article 

    Google Scholar 
    Gramzow, M. et al. Role of phospholipase A2 in the stimulation of sponge cell proliferation by homologous lectin. Cell 59, 939–948 (1989).CAS 
    Article 

    Google Scholar 
    Nomura, T. & Ogata, H. Distribution of prostagladins in the animal kingdom. Biochim. Biophys. Acta 431, 127–131 (1976).CAS 
    Article 

    Google Scholar  More

  • in

    Thicker eggshells are not predicted by host egg ejection behaviour in four species of Australian cuckoo

    Rothstein, S. I. A model system for coevolution: Avian brood parasitism. Annu. Rev. Ecol. Syst. 21, 481–508 (1990).Article 

    Google Scholar 
    Feeney, W. E. et al. Brood parasitism and the evolution of cooperative breeding in birds. Science 342, 1506–1508 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Brooke, M. de L. & Davies, N. B. Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature 335, 630–632 (1988).ADS 
    Article 

    Google Scholar 
    Medina, I. & Langmore, N. E. The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts. Biol. Let. 11, 20150296 (2015).Article 

    Google Scholar 
    Langmore, N. E., Hunt, S. & Kilner, R. M. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422, 157–160 (2003).ADS 
    CAS 
    Article 

    Google Scholar 
    Grim, T. Experimental evidence for chick discrimination without recognition in a brood parasite host. Proc. R. Soc. B: Biol. Sci. 274, 373–381 (2007).Article 

    Google Scholar 
    Sato, N. J., Tokue, K., Noske, R. A., Mikami, O. K. & Ueda, K. Evicting cuckoo nestlings from the nest: A new anti-parasitism behaviour. Biol. Let. 6, 67–69. https://doi.org/10.1098/rsbl.2009.0540 (2010).Article 

    Google Scholar 
    Davies, N. & Brooke, M. de L. Cuckoos versus reed warblers: Adaptations and counteradaptations. Anim. Behav. 36, 262–284 (1988).Article 

    Google Scholar 
    Langmore, N. E. et al. Visual mimicry of host nestlings by cuckoos. Proc. R. Soc. B: Biol. Sci. 278, 2455–2463 (2011).Article 

    Google Scholar 
    Noh, H.-J., Gloag, R. & Langmore, N. E. True recognition of nestlings by hosts selects for mimetic cuckoo chicks. Proc. R. Soc. B: Bio. Sci. 285, 20180726 (2018).Article 

    Google Scholar 
    Spottiswoode, C. N. & Stevens, M. Host-parasite arms races and rapid changes in bird egg appearance. Am. Nat. 179, 633–648. https://doi.org/10.1086/665031 (2012).Article 

    Google Scholar 
    Taylor, C. J. & Langmore, N. E. How do brood-parasitic cuckoos reconcile conflicting environmental and host selection pressures on egg size investment?. Anim. Behav. 168, 89–96. https://doi.org/10.1016/j.anbehav.2020.08.003 (2020).Article 

    Google Scholar 
    Langmore, N. E., Maurer, G., Adcock, G. J. & Kilner, R. M. Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62, 1689–1699 (2008).Article 

    Google Scholar 
    Noh, H. J., Jacomb, F., Gloag, R. & Langmore, N. E. Frontline defences against cuckoo parasitism in the large-billed gerygones. Anim. Behav. 174, 51–61. https://doi.org/10.1016/j.anbehav.2021.01.021 (2021).Article 

    Google Scholar 
    Langmore, N. E. & Kilner, R. M. Why do Horsfield’s bronze-cuckoo Chalcites basalis eggs mimic those of their hosts?. Behav. Ecol. Sociobiol. 63, 1127–1131. https://doi.org/10.1007/s00265-009-0759-9 (2009).Article 

    Google Scholar 
    Spottiswoode, C. N. & Stevens, M. How to evade a coevolving brood parasite: Egg discrimination versus egg variability as host defences. Proc. R. Soc. B: Biol. Sci. 278, 3566–3573. https://doi.org/10.1098/rspb.2011.0401 (2011).Article 

    Google Scholar 
    Yang, C., Wang, L., Liang, W. & Møller, A. P. Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos. Anim. Behav. 122, 177–181. https://doi.org/10.1016/j.anbehav.2016.10.018 (2016).Article 

    Google Scholar 
    Stevens, M. Bird brood parasitism. Curr. Biol. 23, R909–R913. https://doi.org/10.1016/j.cub.2013.08.025 (2013).MathSciNet 
    CAS 
    Article 

    Google Scholar 
    Feeney, W. E., Troscianko, J., Langmore, N. E. & Spottiswoode, C. N. Evidence for aggressive mimicry in an adult brood parasitic bird, and generalized defences in its host. Proc. R. Soc. B: Biol. Sci. 282, 20150795 (2015).Article 

    Google Scholar 
    Davies, N. B. & Welbergen, J. A. Cuckoo–hawk mimicry? An experimental test. Proc. R. Soc. B: Biol. Sci. 275, 1817–1822 (2008).CAS 
    Article 

    Google Scholar 
    Brooker, L. C. & Brooker, M. G. Why are cuckoos host specific?. Oikos 57, 301–309. https://doi.org/10.2307/3565958 (1990).Article 

    Google Scholar 
    Langmore, N. E., Stevens, M., Maurer, G. & Kilner, R. M. Are dark cuckoo eggs cryptic in host nests?. Anim. Behav. 78, 461–468 (2009).Article 

    Google Scholar 
    Lack, D. L. Ecological Adaptations for Breeding in Birds (Methuen & Co., Ltd., 1968).
    Google Scholar 
    Spaw, C. D. & Rohwer, S. A comparative study of eggshell thickness in cowbirds and other passerines. The Condor 89, 307–318. https://doi.org/10.2307/1368483 (1987).Article 

    Google Scholar 
    Igic, B. et al. Alternative mechanisms of increased eggshell hardness of avian brood parasites relative to host species. J. R. Soc. Interface 8, 1654–1664. https://doi.org/10.1098/rsif.2011.0207 (2011).Article 

    Google Scholar 
    Brooker, M. G. & Brooker, L. C. Eggshell strength in cuckoos and cowbirds. Ibis 133, 406–413. https://doi.org/10.1111/j.1474-919X.1991.tb04589.x (1991).Article 

    Google Scholar 
    Maurer, G. et al. First light for avian embryos: eggshell thickness and pigmentation mediate variation in development and UV exposure in wild bird eggs. Funct. Ecol. 29, 209–218 (2015).Article 

    Google Scholar 
    Amos, A. & Rahn, H. Pores in avian eggshells: Gas conductance, gas exchange and embryonic growth rate. Respir. Physiol. 61, 1–20 (1985).Article 

    Google Scholar 
    Ar, A., Rahn, H. & Paganelli, C. V. The avian egg: Mass and strength. Condor 81, 331–337 (1979).Article 

    Google Scholar 
    Rahn, H. & Ar, A. Gas-exchange of the avian egg: Time, structure, and function. Am. Zool. 20, 477–484 (1980).Article 

    Google Scholar 
    Swynnerton, C. Rejections by birds of eggs unlike their own: With remarks on some of the cuckoo problems. Ibis 60, 127–154 (1918).Article 

    Google Scholar 
    López, A. V., Fiorini, V. D., Ellison, K. & Peer, B. D. Thick eggshells of brood parasitic cowbirds protect their eggs and damage host eggs during laying. Behav. Ecol. 29, 965–973 (2018).Article 

    Google Scholar 
    Wyllie, I. The Cuckoo (Batsford, 1981).
    Google Scholar 
    Yang, C. et al. Keeping eggs warm: Thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs. Sci. Nat. 105, 10 (2018).Article 

    Google Scholar 
    Davies, N. B. Cuckoos Cowbirds and other Cheats (T & A D Poyser, 2000).
    Google Scholar 
    Spottiswoode, C. N. The evolution of host-specific variation in cuckoo eggshell strength. J. Evol. Biol. 23, 1792–1799. https://doi.org/10.1111/j.1420-9101.2010.02010.x (2010).CAS 
    Article 

    Google Scholar 
    Langmore, N. E. et al. The evolution of egg rejection by cuckoo hosts in Australia and Europe. Behav. Ecol. 16, 686–692. https://doi.org/10.1093/beheco/ari041 (2005).Article 

    Google Scholar 
    Rohwer, S., Spaw, C. D. & Røskaft, E. Costs to northern orioles of puncture-ejecting parasitic cowbird eggs from their nests. The Auk 106, 734–738 (1989).
    Google Scholar 
    Brooker, M. G., Brooker, L. C. & Rowley, I. Egg deposition by the bronze-cuckoos Chrysococcyx basalis and Chrysococcyx lucidus. Emu 88, 107–109. https://doi.org/10.1071/Mu9880107 (1988).Article 

    Google Scholar 
    McClelland, S. C. et al. Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies. Proc. R. Soc B-Biol. Sci. https://doi.org/10.1098/rspb.2021.1137 (2021).Article 

    Google Scholar 
    Gosler, A. G. & Wilkin, T. A. Eggshell speckling in a passerine bird reveals chronic long-term decline in soil calcium. Bird Study 64, 195–204. https://doi.org/10.1080/00063657.2017.1314448 (2017).Article 

    Google Scholar 
    Lundholm, C. E. Inhibition of prostaglandin synthesis in eggshell gland mucosa as a mechanism for P, P’-DDE-induced eggshell thinning in birds: A comparison of ducks and domestic-fowls. Comp. Biochem. Phys. C 106, 389–394. https://doi.org/10.1016/0742-8413(93)90151-A (1993).Article 

    Google Scholar 
    Bitman, J., Cecil, H. C. & Fries, G. F. DDT-Induced inhibition of avian shell gland carbonic anhydrase: A mechanism for thin eggshells. Science 168, 594–596. https://doi.org/10.1126/science.168.3931.594 (1970).ADS 
    CAS 
    Article 

    Google Scholar 
    Ratcliffe, D. A. Changes attributable to pesticides in egg breakage frequency and eggshell thickness in some British birds. J. Appl. Ecol. 7, 67-+. https://doi.org/10.2307/2401613 (1970).Article 

    Google Scholar 
    Bouwman, H., Govender, D., Underhill, L. & Polder, A. Chlorinated, brominated and fluorinated organic pollutants in African Penguin eggs: 30 years since the previous assessment. Chemosphere 126, 1–10. https://doi.org/10.1016/j.chemosphere.2014.12.071 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    Bleu, J., Agostini, S., Angelier, F. & Biard, C. Experimental increase in temperature affects eggshell thickness, and not egg mass, eggshell spottiness or egg composition in the great tit (Parus major). Gen. Comp. Endocr. 275, 73–81. https://doi.org/10.1016/j.ygcen.2019.02.004 (2019).CAS 
    Article 

    Google Scholar 
    Picman, J. & Pribil, S. Is greater eggshell density an alternative mechanism by which parasitic cuckoos increase the strength of their eggs?. J. Ornithol. 138, 531–541. https://doi.org/10.1007/bf01651384 (1997).Article 

    Google Scholar 
    Lopez, A. V. et al. How to build a puncture- and breakage-resistant eggshell? Mechanical and structural analyses of avian brood parasites and their hosts. J. Exp. Biol. 224, jeb243016. https://doi.org/10.1242/jeb.243016 (2021).Article 

    Google Scholar 
    Soler, M., Rodriguez-Navarro, A. B., Perez-Contreras, T., Garcia-Ruiz, J. M. & Soler, J. J. Great spotted cuckoo eggshell microstructure characteristics can make eggs stronger. J. Avian Biol. 50, e02252. https://doi.org/10.1111/jav.02252 (2019).Article 

    Google Scholar 
    D’Alba, L. et al. Evolution of eggshell structure in relation to nesting ecology in non-avian reptiles. J. Morphol. 282, 1066–1079. https://doi.org/10.1002/jmor.21347 (2021).CAS 
    Article 

    Google Scholar 
    Legendre, L. J. & Clarke, J. A. Shifts in eggshell thickness are related to changes in locomotor ecology in dinosaurs. Evolution 75, 1415–1430. https://doi.org/10.1111/evo.14245 (2021).Article 

    Google Scholar 
    Le Roy, N., Stapane, L., Gautron, J. & Hincke, M. T. Evolution of the avian eggshell biomineralization protein toolkit: New insights from multi-omics. Front. Genet. 12, 672433. https://doi.org/10.3389/fgene.2021.672433 (2021).CAS 
    Article 

    Google Scholar 
    Medina, I. & Langmore, N. E. Batten down the thatches: Front-line defences in an apparently defenceless cuckoo host. Anim. Behav. 112, 195–201. https://doi.org/10.1016/j.anbehav.2015.12.006 (2016).Article 

    Google Scholar 
    Starling, M., Heinsohn, R., Cockburn, A. & Langmore, N. E. Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry. Proc. R. Soc. Lond. B 273, 1929–1934 (2006).CAS 

    Google Scholar 
    Abernathy, V. E., Troscianko, J. & Langmore, N. E. Egg mimicry by the Pacific koel: Mimicry of one host facilitates exploitation of other hosts with similar egg types. J. Avian Biol. 48, 1414–1424. https://doi.org/10.1111/jav.01530 (2017).Article 

    Google Scholar 
    Green, R. E. An evaluation of three indices of eggshell thickness. Ibis 142, 676–679. https://doi.org/10.1111/j.1474-919X.2000.tb04468.x (2000).Article 

    Google Scholar 
    Green, R. E. Long-term decline in the thickness of eggshells of thrushes, Turdus spp., in Britain. Proc. R. Soc. London. Ser. B: Biol. Sci. 265, 679–684. https://doi.org/10.1098/rspb.1998.0347 (1998).Article 

    Google Scholar 
    Igic, B. et al. Comparison of micrometer-and scanning electron microscope-based measurements of avian eggshell thickness. J. Field Ornithol. 81, 402–410 (2010).Article 

    Google Scholar 
    Maurer, G., Portugal, S. J. & Cassey, P. A comparison of indices and measured values of eggshell thickness of different shell regions using museum eggs of 230 European bird species. Ibis 154, 714–724 (2012).Article 

    Google Scholar 
    Becking, J. The ultrastructure of the avian eggshell. Ibis 117, 143–151 (1975).Article 

    Google Scholar 
    Birkhead, T. et al. New insights from old eggs–the shape and thickness of Great Auk Pinguinus impennis eggs. Ibis 162(4), 1345–1354 (2020).Article 

    Google Scholar 
    Riley, A., Sturrock, C., Mooney, S. & Luck, M. Quantification of eggshell microstructure using X-ray micro computed tomography. Br. Poult. Sci. 55, 311–320 (2014).CAS 
    Article 

    Google Scholar 
    Kibala, L., Rozempolska-Rucinska, I., Kasperek, K., Zieba, G. & Lukaszewicz, M. Ultrasonic eggshell thickness measurement for selection of layers. Poult. Sci. 94, 2360–2363. https://doi.org/10.3382/ps/pev254 (2015).Article 

    Google Scholar 
    Khaliduzzaman, A. et al. A nondestructive eggshell thickness measurement technique using terahertz waves. Sci. Rep. 10, 1–5 (2020).Article 

    Google Scholar 
    Santolo, G. M. A new nondestructive method for measuring eggshell thickness using a non-ferrous material thickness gauge. Wilson J. Ornithol. 130, 502–509. https://doi.org/10.1676/17-035.1 (2018).Article 

    Google Scholar 
    Marini, M. A. et al. The five million bird eggs in the world’s museum collections are an invaluable and underused resource. Auk 137, ukaa036. https://doi.org/10.1093/auk/ukaa036 (2020).Article 

    Google Scholar 
    Brooker, M. G. & Brooker, L. C. Cuckoo hosts in Australia. Aust. Zool. Rev. 2, 1–67 (1989).
    Google Scholar 
    Higgins, P. J. Vol. Volume 4: Parrots to Dollarbird (Oxford University Press, 1999).
    Google Scholar 
    Higgins, P. J. & Peter, J. M. Vol. 6: Pardalotes to Shrike-Thrushes (Oxford University Press, 2002).
    Google Scholar 
    Higgins, P. J., Peter, J. M. & Cowling, S. J. Vol. 4: Parrots to Dollarbird (Oxford University Press, 2006).
    Google Scholar 
    Higgins, P. J., Peter, J. M. & Steele, W. K. Vol. 5: Tyrant-flycatchers to Chats (Oxford University Press, 2001).
    Google Scholar 
    Landstrom, M., Heinsohn, R. & Langmore, N. E. Clutch variation and egg rejection in three hosts of the pallid cuckoo Cuculus pallidus. Behaviour 147, 19–36. https://doi.org/10.1163/000579509X12483520922043 (2010).Article 

    Google Scholar 
    Abernathy, V. E., Johnson, L. E. & Langmore, N. E. An experimental test of defenses against avian brood parasitism in a recent host. Front. Ecol. Evol. 9, 244. https://doi.org/10.3389/fevo.2021.651733 (2021).Article 

    Google Scholar 
    Landstrom, M. T., Heinsohn, R. & Langmore, N. E. Does clutch variability differ between populations of cuckoo hosts in relation to the rate of parasitism?. Anim. Behav. 81, 307–312 (2011).Article 

    Google Scholar 
    Peterson, S. H. et al. Avian eggshell thickness in relation to egg morphometrics, embryonic development, and mercury contamination. Ecol. Evol. 10, 8715–8740. https://doi.org/10.1002/ece3.6570 (2020).Article 

    Google Scholar 
    Attard, M., Medina, I., Langmore, N. E. & Sherratt, E. Egg shape mimicry in parasitic cuckoos. J. Evol. Biol. 30, 2079–2084 (2017).CAS 
    Article 

    Google Scholar 
    Birchard, G. F. & Deeming, D. C. Avian eggshell thickness: Scaling and maximum body mass in birds. J. Zool. 279, 95–101. https://doi.org/10.1111/j.1469-7998.2009.00596.x (2009).Article 

    Google Scholar 
    Orme, D. et al. The caper package: Comparative analysis of phylogenetics and evolution in R. R Packag. Vers. 5, 549–593 (2013).
    Google Scholar 
    Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448. https://doi.org/10.1038/nature11631 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    Schliep, K. P. Phangorn: Phylogenetic analysis in R. Bioinformatics 27, 592–593. https://doi.org/10.1093/bioinformatics/btq706 (2011).CAS 
    Article 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing, (2013). More

  • in

    Habitat preferences, estimated abundance and behavior of tree hyrax (Dendrohyrax sp.) in fragmented montane forests of Taita Hills, Kenya

    Fischer, R. et al. Accelerated forest fragmentation leads to critical increase in tropical forest edge area. Sci. Adv. 7, eabg7012 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    Newmark, W. D. & McNeally, P. B. Impact of habitat fragmentation on the spatial structure of the Eastern Arc forests in East Africa: Implications for biodiversity conservation. Biodivers. Conserv. 27, 1387–1402 (2018).Article 

    Google Scholar 
    Hall, J., Burgess, N. D., Lovett, J., Mbilinyi, B. & Gereau, R. E. Conservation implications of deforestation across an elevational gradient in the Eastern Arc Mountains, Tanzania. Biol. Conserv. 142, 2510–2521 (2009).Article 

    Google Scholar 
    Kuussaari, M. et al. Extinction debt: A challenge for biodiversity conservation. Trends Ecol. Evol. 24, 564–571 (2009).Article 

    Google Scholar 
    Gibson, L. et al. Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341, 1508–1510 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Burgess, N. D. et al. The biological importance of the Eastern Arc Mountains of Tanzania and Kenya. Biol. Conserv. 134, 209–231 (2007).Article 

    Google Scholar 
    Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    Oates, J. F. et al. A new species of tree hyrax (Procaviidae: Dendrohyrax) from West Africa and the significance of the Niger-Volta interfluvium in mammalian biogeography. Zool. J. Linn. Soc. 194, 527–552 (2022).Article 

    Google Scholar 
    Bloomer, P. Extant hyrax diversity is vastly underestimated. Afrotherian. Conserv. 7, 11–16 (2009).
    Google Scholar 
    Roberts, D., Topp-Jørgensen, E. & Moyer, D. C. Dendrohyrax validus Eastern Tree Hyrax. In Mammals of Africa Vol. I (eds Kingdon, J. et al.) 158–161 (Bloomsbury, 2013).
    Google Scholar 
    Hoeck, H. Some thoughts on the distribution of the tree hyraxes (genus Dendrohyrax) in northern Tanzania. Afrotherian Conserv. 13, 47–49 (2017).
    Google Scholar 
    Rosti, H., Pihlström, H., Bearder, S., Pellikka, P. & Rikkinen, J. Vocalization analyses of nocturnal arboreal mammals of the Taita Hills, Kenya. Diversity 12, 473 (2020).Article 

    Google Scholar 
    Roberts, D. Geographic variation in the loud calls of tree hyrax – Dendrohyrax validus (True 1890) In the Eastern Arc Mountains, East Africa: taxonomic and conservation implications. (MSc thesis, University of Reading, 2001).True, F. W. Description of two new species of mammals from Mt. Kilima-Njaro, East Africa. Proc. US Nat. Mus. 13, 227–229 (1890).Article 

    Google Scholar 
    True, F. W. An annotated catalogue of the mammals collected by Dr. W. L. Abbott in the Kilma-Njaro region, East Africa. Proc. U. S. Nat. Mus. 15, 445–480 (1892).Article 

    Google Scholar 
    Kundaeli, J. N. Distribution of tree hyrax (Dendrohyrax validus validus True) on Mt Kilimanjaro, Tanzania. Afr. J. Ecol. 14, 253–264 (1976).Article 

    Google Scholar 
    Gaylard, A. & Kerley, G. I. H. Diet of tree hyraxes Dendrohyrax arboreus (Hyracoidea: Procaviidae) in the Eastern Cape, South Africa. J. Mammal. 78, 213–221 (1997).Article 

    Google Scholar 
    Milner, J. Relationships between the forest dwelling people of south-west Mau and tree hyrax, Dendrohyrax arboreus. J. East Afr. Nat. Hist. 83, 17–29 (1994).Article 

    Google Scholar 
    Milner, J. M. & Harris, S. Habitat use and ranging behaviour of tree hyrax, Dendrohyrax arboreus, in the Virunga Volcanoes, Rwanda. Afr. J. Ecol. 37, 281–294 (1999).Article 

    Google Scholar 
    Gaylard, A. & Kerley, G. I. H. Habitat assessment for a rare, arboreal forest mammal, the tree hyrax (Dendrohyrax arboreus). Afr. J. Ecol. 39, 205–212 (2001).Article 

    Google Scholar 
    Djossa, B., Zachee, B. & Sinzin, B. Activity patterns and habitat use of the western tree hyrax (Dendrohyrax dorsalis), within forest patches and implications for conservation. Ecotropica 18, 65–72 (2012).
    Google Scholar 
    Opperman, E. J., Cherry, M. I. & Makunga, N. P. Community harvesting of trees used as dens and for food by the tree hyrax (Dendrohyrax arboreus) in the Pirie forest, South Africa. Koedoe 60, a1481 (2018).
    Cordeiro, N. J. et al. Notes on the ecology and status of some forest mammals in four Eastern Arc Mountains, Tanzania. J. East Afr. Nat. Hist. 94, 175–189 (2005).Article 

    Google Scholar 
    Koren, L. Vocalization as an indicator of individual quality in the rock hyrax. (PhD thesis, Tel-Aviv University, 2006).Koren, L., Mokady, O. & Geffen, E. Social status and cortisol levels in singing rock hyraxes. Horm. Behav. 54, 212–216 (2008).CAS 
    Article 

    Google Scholar 
    Koren, L. & Geffen, E. Complex call in male rock hyrax (Procavia capensis): A multi-information distributing channel. Behav. Ecol. Sociobiol. 63, 581–590 (2009).Article 

    Google Scholar 
    Lawes, M. J., Mealin, P. E. & Piper, S. E. Patch occupancy and potential metapopulation dynamics of three forest mammals in fragmented Afromontane forest in South Africa. Conserv. Biol. 14, 1088–1098 (2000).Article 

    Google Scholar 
    Topp-Jørgensen, J. E., Marshal, A. R., Brink, H. & Pedersen, U. B. Quantifying the response of tree hyraxes (Dendrohyrax validus) to human disturbance in the Udzungwa Mountains, Tanzania. Trop. Conserv. Sci. 1, 63–74 (2008).Article 

    Google Scholar 
    Hill, A. P. et al. AudioMoth: Evaluation of a smart open acoustic device for monitoring biodiversity and the environment. Methods Ecol. Evol. 9, 1199–1211 (2018).Article 

    Google Scholar 
    Marques, T. A. et al. Estimating animal population density using passive acoustics. Biol. Rev. 88, 287–309 (2013).Article 

    Google Scholar 
    Pérez-Granados, C. & Traba, J. Estimating bird density using passive acoustic monitoring: A review of methods and suggestions for further research. Ibis 163, 765–783 (2021).Article 

    Google Scholar 
    Campos-Cerqueira, M. & Aide, T. M. Improving distribution data of threatened species by combining acoustic monitoring and occupancy modelling. Methods Ecol. Evol. 7, 1340–1348 (2016).Article 

    Google Scholar 
    McLean, K. A. et al. Movement patterns of three arboreal primates in a Neotropical moist forest explained by LiDAR-estimated canopy structure. Landsc. Ecol. 31, 1849–1862 (2016).Article 

    Google Scholar 
    Davies, A. B., Ancrenaz, M., Oram, F. & Asner, G. P. Canopy structure drives orangutan habitat selection in disturbed Bornean forests. Proc. Natl. Acad. Sci. USA 114, 8307–8312 (2017).CAS 
    Article 

    Google Scholar 
    Singh, M., Cheyne, S. M. & Ehlers Smith, D. A. How conspecific primates use their habitats: Surviving in an anthropogenically-disturbed forest in Central Kalimantan, Indonesia. Ecol. Indic. 87, 167–177 (2018).Article 

    Google Scholar 
    Simonson, W. D., Allen, H. D. & Coomes, D. A. Applications of airborne lidar for the assessment of animal species diversity. Methods Ecol. Evol. 5, 719–729 (2014).Article 

    Google Scholar 
    Aerts, R. et al. Woody plant communities of isolated Afromontane cloud forests in Taita Hills, Kenya. Plant Ecol. 212, 639–649 (2011).Article 

    Google Scholar 
    Lovett, J. C., Wasser, S. K., Cambridge University Press. Biogeography and Ecology of the Rain Forests of Eastern Africa (Cambridge University Press, 2008).
    Google Scholar 
    Pellikka, P. K. E., Lötjönen, M., Siljander, M. & Lens, L. Airborne remote sensing of spatiotemporal change (1955–2004) in indigenous and exotic forest cover in the Taita Hills, Kenya. Int. J. Appl. Earth Obs. Geoinf. 11, 221–232 (2009).ADS 
    Article 

    Google Scholar 
    Rovero, F. et al. Targeted vertebrate surveys enhance the faunal importance and improve explanatory models within the Eastern Arc Mountains of Kenya and Tanzania. Diversity Distrib. 20, 1438–1449 (2014).Article 

    Google Scholar 
    Rosti, H., Rikkinen, J., Pellikka, P., Bearder, S. & Mwamodenyi, J. M. Taita Mountain dwarf galago is extant in the Taita Hills of Kenya. Oryx 54, 152–153 (2020).Article 

    Google Scholar 
    Pihlström, H., Rosti, H., Lombo, B. & Pellikka, P. Domestic dog predation on white-tailed small-eared galago (Otolemur garnettii lasiotis) in the Taita Hills, Kenya. Afr. Primates 15, 31–38 (2021).
    Google Scholar 
    Etana, B. et al. Traditional shade coffee forest systems act as refuges for medium- and large-sized mammals as natural forest dwindles in Ethiopia. Biol. Conserv. 260, 109219 (2021).Article 

    Google Scholar 
    Hoeck, H., Rovero, F., Cordeiro, N., Butynski, T., Perkin, A. & Jones, T. Dendrohyrax validus. The IUCN Red List of Threatened Species (2015: e.T136599A21288090).Himberg, N. Traditionally protected forests’ role within transforming natural resource management regimes in Taita Hills, Kenya. (PhD thesis, University of Helsinki, 2011).Thijs, K. W., Roelen, I. & Musila, W. M. Field guide to the woody plants of Taita Hills, Kenya. J. East Afr. Nat. Hist. 102, 1–272 (2014).Article 

    Google Scholar 
    Yéboué, K. Y. et al. Genetic typing and in silico assignment of smoked and fresh bushmeat sold on markets and restaurants in west-central Côte d’Ivoire. Int. J. Genet. Mol. Biol. 13, 1–8 (2021).Article 

    Google Scholar 
    Brown, K. J. & Downs, C. T. Seasonal behavioural patterns of free-living rock hyrax (Procavia capensis). J. Zool. 265, 311–326 (2005).Article 

    Google Scholar 
    Brown, K. J. & Downs, C. T. Seasonal patterns in body temperature of free-living rock hyrax (Procavia capensis). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 143, 42–49 (2006).Article 

    Google Scholar 
    Ilany, A., Barocas, A., Kam, M., Ilany, T. & Geffen, E. The energy cost of singing in wild rock hyrax males: Evidence for an index signal. Anim. Behav. 85, 995–1001 (2013).Article 

    Google Scholar 
    Demartsev, V. et al. Male hyraxes increase song complexity and duration in the presence of alert individuals. Behav. Ecol. 25, 1451–1458 (2014).Article 

    Google Scholar 
    Gaynor, K. M., Hojnowski, C. E., Carter, N. H. & Brashares, J. S. The influence of human disturbance on wildlife nocturnality. Science 360, 1232–1235 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Adhikari, H. et al. Determinants of aboveground biomass across an Afromontane landscape mosaic in Kenya. Remote Sens. 9, 827 (2017).ADS 
    Article 

    Google Scholar 
    Heiskanen, J., Korhonen, L., Hietanen, J. & Pellikka, P. K. E. Use of airborne lidar for estimating canopy gap fraction and leaf area index of tropical montane forests. Int. J. Remote Sens. 36, 2569–2583 (2015).Article 

    Google Scholar 
    Roussel, J.-R. et al. lidR: An R package for analysis of Airborne Laser Scanning (ALS) data. Remote Sens. Environ. 251, 112061 (2020).ADS 
    Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).
    Google Scholar 
    Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378 (2017).Article 

    Google Scholar 
    Lüdecke, D., Ben-Shachar, M., Patil, I., Waggoner, P. & Makowski, D. Performance: An R package for assessment, comparison and testing of statistical models. JOSS 6, 3139 (2021).ADS 
    Article 

    Google Scholar 
    Wickham, H. Ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).MATH 
    Book 

    Google Scholar 
    Zuur, A. F., Savelʹev, A. A. & Ieno, E. N. Zero Inflated Models and Generalized Linear Mixed Models with R (Highland Statistics, 2012).
    Google Scholar 
    Campbell, H. The consequences of checking for zero-inflation and overdispersion in the analysis of count data. Methods Ecol. Evol. 12, 665–680 (2021).Article 

    Google Scholar 
    Zuur, A. F. & Ieno, E. N. A protocol for conducting and presenting results of regression-type analyses. Methods Ecol. Evol. 7, 636–645 (2016).Article 

    Google Scholar 
    Aho, K., Derryberry, D. & Peterson, T. Model selection for ecologists: The worldviews of AIC and BIC. Ecology 95, 631–636 (2014).Article 

    Google Scholar  More

  • in

    Four millennia of long-term individual foraging site fidelity in a highly migratory marine predator

    Oppel, S. et al. Spatial scales of marine conservation management for breeding seabirds. Mar. Policy 98, 37–46 (2018).Article 

    Google Scholar 
    Lewison, R. et al. Research priorities for seabirds: improving conservation and management in the 21st century. Endanger. Species Res 17, 93–121 (2012).Article 

    Google Scholar 
    Hasegawa, H. & DeGange, A. R. The Short-tailed Albatross, Diomedea albatrus, its status, distribution and natural history. Am. Birds 36, 806–814 (1982).
    Google Scholar 
    Tickell, W. L. N. Albatrosses (Pica Press, 2000).BirdLife International. Phoebastria albatrus. The IUCN Red List of Threatened Species, e.T22698335A132642113 https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22698335A132642113.en (2018).Japan Ministry of the Environment. Ministry of the Environment Red List (Government of Japan, 2020).COSEWIC. COSEWIC Assessment and Status Report on the Short-tailed Albatross Phoebastria albatrus in Canada (Committee on the Status of Endangered Wildlife in Canada, 2013).Environment Canada. Recovery Strategy for the Short-tailed Albatross (Phoebastria albatrus) and the Pink-footed Shearwater (Puffinus creatopus) in Canada (Environment Canada, 2008).United States of America Fish and Wildlife Service. Endangered and Threatened Wildlife and Plants; Final Rule to List the Short-tailed Albatross as Endangered in the United States. 65 FR 46643, 46643–4654, Document Number 00–19123 (2000).United States of America Fish and Wildlife Service. Short-tailed Albatross (Phoebastria albatrus) 5-Year Review: Summary and Evaluation (United States of America Fish and Wildlife Service, 2020).United States of America Fish and Wildlife Service. Short-tailed Albaross Recovery Plan (United States of America Fish and Wildlife Service, 2008).Orben, R. A. et al. Ontogenetic changes in at-sea distributions of immature short-tailed albatrosses Phoebastria albatrus. Endanger. Species Res 35, 23–37 (2018).Article 

    Google Scholar 
    Orben, R. A. et al. Across borders: external factors and prior behaviour influence North Pacific albatross associations with fishing vessels. J. Appl. Ecol. 58, 1272–1283 (2021).Article 

    Google Scholar 
    Fox, C. H., Robertson, C., O’Hara, P. D., Tadey, R. & Morgan, K. H. Spatial assessment of albatrosses, commercial fisheries, and bycatch incidents on Canada’s Pacific coast. Mar. Ecol. Prog. Ser. 672, 205–222 (2021).Article 

    Google Scholar 
    Piatt, J. F. et al. Predictable hotspots and foraging habitat of the endangered short-tailed albatross (Phoebastria albatrus) in the North Pacific: implications for conservation. Deep Sea Res. Part II 53, 387–398 (2006).Article 

    Google Scholar 
    Suryan, R. M. et al. Migratory routes of short-tailed albatrosses: use of exclusive economic zones of North Pacific Rim countries and spatial overlap with commercial fisheries in Alaska. Biol. Conserv. 137, 450–460 (2007).Article 

    Google Scholar 
    Suryan, R. M. & Fischer, K. N. Stable isotope analysis and satellite tracking reveal interspecific resource partitioning of nonbreeding albatrosses off Alaska. Can. J. Zool. 88, 299–305 (2010).CAS 
    Article 

    Google Scholar 
    Zador, S. G., Punt, A. E. & Parrish, J. K. Population impacts of endangered short-tailed albatross bycatch in the Alaskan trawl fishery. Biol. Conserv. 141, 872–882 (2008).Article 

    Google Scholar 
    Geernaert, T. O., Gilroy, H. L., Kaimmer, S. M., Williams, G. H. & Trumble, R. J. A Feasibility Study that Investigates Options for Monitoring Bycatch of the Short-tailed Albatross in the Pacific Halibut Fishery off Alaska (International Pacific Halibut Commission, 2001).Guy, T. J. et al. Overlap of North Pacific albatrosses with the U.S. west coast groundfish and shrimp fisheries. Fish. Res. 147, 222–234 (2013).Article 

    Google Scholar 
    Bolnick, D. I. et al. The ecology of individuals: incidence and implications of individual specialization. Am. Natural 161, 1–28 (2003).Article 

    Google Scholar 
    Votier, S. C. et al. Individual responses of seabirds to commercial fisheries revealed using GPS tracking, stable isotopes and vessel monitoring systems. J. Appl. Ecol. 47, 487–497 (2010).Article 

    Google Scholar 
    Wakefield, E. D. et al. Long-term individual foraging site fidelity—why some gannets don’t change their spots. Ecology 96, 3058–3074 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Votier, S. C. et al. Effects of age and reproductive status on individual foraging site fidelity in a long-lived marine predator. Proc. R. Soc. B 284, 20171068 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sztukowski, L. A. et al. Sex differences in individual foraging site fidelity of Campbell albatross. Mar. Ecol. Prog. Ser. 601, 227–238 (2018).Article 

    Google Scholar 
    Gutowsky, S. E. et al. Divergent post-breeding distribution and habitat associations of fledgling and adult Black-footed Albatrosses Phoebastria nigripes in the North Pacific. Ibis 156, 60–72 (2014).Article 

    Google Scholar 
    Weimerskirch, H., Åkesson, S. & Pinaud, D. Postnatal dispersal of wandering albatrosses Diomedea exulans: implications for the conservation of the species. J. Avian Biol. 37, 23–28 (2006).
    Google Scholar 
    Olson, S. L. & Hearty, P. J. Probable extirpation of a breeding colony of Short-tailed Albatross (Phoebastria albatrus) on Bermuda by Pleistocene sea-level rise. Proc. Natl Acad. Sci. 100, 12825–12829 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dall, W. H. Notes on pre-historic remains in the Aleutian islands. Proc. Calif. Acad. Sci. 4, 283–287 (1872).
    Google Scholar 
    Eda, M. et al. Inferring the ancient population structure of the vulnerable albatross Phoebastria albatrus, combining ancient DNA, stable isotope, and morphometric analyses of archaeological samples. Conserv. Genet. 13, 143–151 (2012).Article 

    Google Scholar 
    Cousins, K. L., Dalzell, P. & Gilman, E. Managing pelagic longline-albatross interactions in the North Pacific Ocean. Mar. Ornithol 28, 159–174 (2000).
    Google Scholar 
    Hobson, K. A. & Montevecchi, W. A. Stable isotopic determinations of trophic relationships of great auks. Oecologia 87, 528–531 (1991).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Fuller, B. T. et al. Pleistocene paleoecology and feeding behavior of terrestrial vertebrates recorded in a pre-LGM asphaltic deposit at Rancho La Brea, California. Palaeogeogr. Palaeoclimatol. Palaeoecol. 537, 109383 (2020).Article 

    Google Scholar 
    Hobson, K. A. & Clark, R. G. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94, 181–188 (1992).Article 

    Google Scholar 
    Hyland, C., Scott, M. B., Routledge, J. & Szpak, P. Stable carbon and nitrogen isotope variability of bone collagen to determine the number of isotopically distinct specimens. J. Archaeol. Method Theory https://doi.org/10.1007/s10816-021-09533-7 (2021).Article 

    Google Scholar 
    Hedges, R. E. M., Clement, J. G., Thomas, D. L. & O’Connell, T. C. Collagen turnover in the adult femoral mid‐shaft: modeled from anthropogenic radiocarbon tracer measurements. Am. J. Phys. Anthropol. 133, 808–816 (2007).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Guiry, E. J., Orchard, T. J., Royle, T. C. A., Cheung, C. & Yang, D. Y. Dietary plasticity and the extinction of the passenger pigeon (Ectopistes migratorius). Quat. Sci. Rev. 233, 106225 (2020).Article 

    Google Scholar 
    Minagawa, M. & Wada, E. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim. Cosmochim. Acta 48, 1135–1140 (1984).CAS 
    Article 

    Google Scholar 
    DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495–506 (1978).CAS 
    Article 

    Google Scholar 
    Hobson, K. A., Ambrose, W. G. Jr & Renaud, P. E. Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Mar. Ecol. Prog. Ser. 128, 1–10 (1995).Article 

    Google Scholar 
    Sigman, D., Karsh, K. & Casciotti, K. Ocean process tracers: nitrogen isotopes in the ocean in Encyclopedia of Ocean Science (eds Steele, J. H. et al.) 4139–4152 (Academic Press, 2009).Guiry, E. Complexities of stable carbon and nitrogen isotope biogeochemistry in ancient freshwater ecosystems: implications for the study of past subsistence and environmental change. Front. Ecol. Evol 7, 313 (2019).Article 

    Google Scholar 
    Rau, G. H., Takahashi, T. & Des Marais, D. J. Latitudinal variations in plankton δ13C: implications for CO2 and productivity in past oceans. Nature 341, 516–518 (1989).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Popp, B. N. et al. Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochim. Cosmochim. Acta 62, 69–77 (1998).CAS 
    Article 

    Google Scholar 
    Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C. & Macko, S. A. Dependence of phytoplankton carbon isotopic composition on growth rate and (CO2) aq: theoretical considerations and experimental results. Geochim. Cosmochim. Acta 59, 1131–1138 (1995).CAS 
    Article 

    Google Scholar 
    Vokhshoori, N. L. et al. Broader foraging range of ancient short-tailed albatross populations into California coastal waters based on bulk tissue and amino acid isotope analysis. Mar. Ecol. Prog. Ser. 610, 1–13 (2019).CAS 
    Article 

    Google Scholar 
    Sherwood, O. A., Lehmann, M. F., Schubert, C. J., Scott, D. B. & McCarthy, M. D. Nutrient regime shift in the western North Atlantic indicated by compound-specific δ15N of deep-sea gorgonian corals. Proc. Natl Acad. Sci. 108, 1011–1015 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Szpak, P., Savelle, J. M., Conolly, J. & Richards, M. P. Variation in late holocene marine environments in the Canadian Arctic Archipelago: evidence from ringed seal bone collagen stable isotope compositions. Quat. Sci. Rev. 211, 136–155 (2019).Article 

    Google Scholar 
    Guiry, E. J. et al. Deforestation caused abrupt shift in Great Lakes nitrogen cycle. Limnol. Oceanogr. 65, 1921–1935 (2020).CAS 
    Article 

    Google Scholar 
    Wiley, A. E. et al. Millennial-scale isotope records from a wide-ranging predator show evidence of recent human impact to oceanic food webs. Proc. Natl Acad. Sci. 110, 8972–8977 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Keeling, C. D. The Suess effect: 13Carbon-14Carbon interrelations. Environ. Int. 2, 229–300 (1979).CAS 
    Article 

    Google Scholar 
    McMahon, K. W., Thorrold, S. R., Elsdon, T. S. & McCarthy, M. D. Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol. Oceanogr. 60, 1076–1087 (2015).CAS 
    Article 

    Google Scholar 
    Chikaraishi, Y. et al. Determination of aquatic food‐web structure based on compound‐specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr. Methods 7, 740–750 (2009).CAS 
    Article 

    Google Scholar 
    Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER–stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Ambrose, S. H. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 17, 431–451 (1990).Article 

    Google Scholar 
    Guiry, E. J. & Szpak, P. Improved quality control criteria for stable carbon and nitrogen isotope measurements of ancient bone collagen. J. Archaeol. Sci. 132, 105416 (2021).CAS 
    Article 

    Google Scholar 
    Thompson, D. R. & Furness, R. W. Stable-isotope ratios of carbon and nitrogen in feathers indicate seasonal dietary shifts in Northern Fulmars. Auk 112, 493–498 (1995).Article 

    Google Scholar 
    Carter, H. R. & Sealy, S. G. Historical occurrence of the short-tailed Albatross in British Columbia and Washington. 1841–1958. Wildl. Afield 11, 24–38 (2014).
    Google Scholar 
    Crockford, S. The Archaeological History of Short-tailed Albatross in British Columbia: A Review and Summary of STAL Skeletal Remains, as Compared to Other Avian Species, Identified from Historic and Prehistoric Midden Deposits. Report on file, Canadian Wildlife Service (2003).Borrmann, R. M., Phillips, R. A., Clay, T. A. & Garthe, S. High foraging site fidelity and spatial segregation among individual great black-backed gulls. J. Avian Biol. 50, e02156 (2019).Article 

    Google Scholar 
    Wilkinson, B. P., Haynes-Sutton, A. M., Meggs, L. & Jodice, P. G. High spatial fidelity among foraging trips of Masked Boobies from Pedro Cays, Jamaica. PLoS ONE 15, e0231654 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Araújo, M. S., Bolnick, D. I. & Layman, C. A. The ecological causes of individual specialisation. Ecol. Lett. 14, 948–958 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Grémillet, D. et al. Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of Cape gannets from neighbouring colonies. Mar. Ecol. Prog. Ser. 268, 265–279 (2004).Article 

    Google Scholar 
    Irons, D. B. Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79, 647–655 (1998).Article 

    Google Scholar 
    Piper, W. H. Making habitat selection more “familiar”: a review. Behav. Ecol. Sociobiol. 65, 1329–1351 (2011).Article 

    Google Scholar 
    Davoren, G. K., Montevecchi, W. A. & Anderson, J. T. Search strategies of a pursuit‐diving marine bird and the persistence of prey patches. Ecol. Monogr. 73, 463–481 (2003).Article 

    Google Scholar 
    Hazen, E. L. et al. Marine top predators as climate and ecosystem sentinels. Front. Ecol. Environ. 17, 565–574 (2019).Article 

    Google Scholar 
    Dall, S. R. X., Bell, A. M., Bolnick, D. I. & Ratnieks, F. L. An evolutionary ecology of individual differences. Ecol. Lett. 15, 1189–1198 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McAllister, N. M. Avian fauna from the Yuquot excavation in The Yuquot Project, Volume 2 (eds. Folan, W. J. & Dewhirst, J.) 103–174 (National Historic Parks and Sites Branch, 1980).Drucker, P. I. The Northern and Central Nootkan tribes. Bureau of American Ethnology Bulletin 144, 1–480 (1951).
    Google Scholar 
    Lepofsky, D. & Caldwell, M. Indigenous marine resource management on the Northwest Coast of North America. Ecol. Process 2, 12 (2013).Article 

    Google Scholar 
    Dewhirst, J. The Indigenous Archaeology of Yuquout, a Nootkan Outside Village (National Historic Parks and Sites Branch, 1980).Longin, R. New method of collagen extraction for radiocarbon dating. Nature 230, 241–242 (1971).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Guiry, E. J. & Hunt, B. P. V. Integrating fish scale and bone isotopic compositions for ‘deep time’ retrospective studies. Mar. Environ. Res. 160, 104982 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Hobson, K. A., Atwell, L. & Wassenaar, L. I. Influence of drinking water and diet on the stable-hydrogen isotope ratios of animal tissues. Proc. Natl Acad. Sci. 96, 8003–8006 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Qi, H., Coplen, T. B., Geilmann, H., Brand, W. A. & Böhlke, J. K. Two new organic reference materials for δ13C and δ15N measurements and a new value for the δ13C of NBS 22 oil. Rapid Commun. Mass Spectrom 17, 2483–2487 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Qi, H. et al. A new organic reference material, l-glutamic acid, USGS41a, for δ13C and δ15N measurements − a replacement for USGS41. Rapid Commun. Mass Spectrom 30, 859–866 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    Szpak, P., Metcalfe, J. Z. & Macdonald, R. A. Best practices for calibrating and reporting stable isotope measurements in archaeology. J. Archaeol. Sci. Rep 13, 609–616 (2017).
    Google Scholar 
    Hammer, Ø., Haper, A. T. & Ryan, P. D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 4 (2001).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).RStudio Team. RStudio: Integrated Development for R (RStudio, PBC, 2019). More

  • in

    Recent expansion of oil palm plantations into carbon-rich forests

    Xu, Y. et al. Annual oil palm plantation maps in Malaysia and Indonesia from 2001 to 2016. Earth Syst. Sci. Data 12, 847–867 (2020).Article 

    Google Scholar 
    Meijaard, E. et al. The environmental impacts of palm oil in context. Nat. Plants 6, 1418–1426 (2020).Article 

    Google Scholar 
    Guillaume, T. et al. Carbon costs and benefits of Indonesian rainforest conversion to plantations. Nat. Commun. 9, 2388 (2018).Article 

    Google Scholar 
    Ordway, E. M. & Asner, G. P. Carbon declines along tropical forest edges correspond to heterogeneous effects on canopy structure and function. Proc. Natl Acad. Sci. USA 117, 7863–7870 (2020).CAS 
    Article 

    Google Scholar 
    Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850 (2013).CAS 
    Article 

    Google Scholar 
    Santoro, M. et al. The global forest above-ground biomass pool for 2010 estimated from high-resolution satellite observations. Earth Syst. Sci. Data 13, 3927–3950 (2021).Article 

    Google Scholar 
    The World Database on Protected Areas (WDPA) (UNEP-WCMC and IUCN, accessed 12 February 2020); www.protectedplanet.netMahmud, A., Rehrig, M. & Hills, G. Improving the Livelihoods of Palm Oil Smallholders: The Role of the Private Sector (FSG, 2010).Lasco, R. Forest carbon budgets in Southeast Asia following harvesting and land cover change. Sci. China 45, 55–64 (2002).Article 

    Google Scholar 
    Historical Greenhouse Gas Emissions (Climate Watch, accessed 6 October 2021); https://www.climatewatchdata.org/Euler, M., Schwarze, S., Siregar, H. & Qaim, M. Oil palm expansion among smallholder farmers in Sumatra, Indonesia. J. Agric. Econ. 67, 658–676 (2016).Article 

    Google Scholar 
    Donofrio, S., Rothrock, P. & Leonard, J. J. F. T. Supply Change: Tracking Corporate Commitments to Deforestation-free SupplyChains, 2017 (Forest Trends, 2017).Rist, L., Feintrenie, L. & Levang, P. The livelihood impacts of oil palm: smallholders in Indonesia. Biodivers. Conserv. 19, 1009–1024 (2010).Article 

    Google Scholar 
    Saadun, N. et al. Socio-ecological perspectives of engaging smallholders in environmental-friendly palm oil certification schemes. Land Use Policy 72, 333–340 (2018).Article 

    Google Scholar 
    Hansen, M. C., Stehman, S. V. & Potapov, P. V. Quantification of global gross forest cover loss. Proc. Natl Acad. Sci. USA 107, 8650 (2010).CAS 
    Article 

    Google Scholar 
    Santoro, M. & Cartus, O. ESA Biomass Climate Change Initiative (Biomass_cci): Global datasets of forest above-ground biomass for the year 2017 v.1 (Centre for Environmental Data Analysis, 2019); https://doi.org/10.5285/bedc59f37c9545c981a839eb552e4084Busch, J. et al. Reductions in emissions from deforestation from Indonesia’s moratorium on new oil palm, timber, and logging concessions. Proc. Natl Acad. Sci. USA 112, 1328–1333 (2015).CAS 
    Article 

    Google Scholar 
    McGarigal, K., Cushman, S. A. & Ene, E. FRAGSTATS v.4: spatial pattern analysis program for categorical and continuous maps (Univ. Massachusetts, 2012). More

  • in

    Elevated extinction risk of cacti under climate change

    Boyle, T. H. & Anderson, E. in Cacti: Biology and Uses (ed. Nobel, P. S.) 125–141 (Univ. California Press, 2002).Gibson, A. C. & Nobel, P. S. The Cactus Primer (Harvard Univ. Press, 1986).Bravo Hollis, H. & Sánchez Mejorada, H. Las Cactáceas de México (Univ. Nacional Autónoma de México, 1978).Goettsch, B. et al. High proportion of cactus species threatened with extinction. Nat. Plants 1, 15142 (2015).CAS 
    PubMed 

    Google Scholar 
    Benavides, E., Breceda, A. & Anadón, J. D. Winners and losers in the predicted impact of climate change on cacti species in Baja California. Plant Ecol. 222, 29–44 (2021).
    Google Scholar 
    Nobel, P. S. Responses of some North American CAM plants to freezing temperatures and doubled CO2 concentrations: implications of global climate change for extending cultivation. J. Arid. Environ. 34, 187–196 (1996).
    Google Scholar 
    Reyes-García, C. & Andrade, J. L. Crassulacean acid metabolism under global climate change. N. Phytol. 181, 754–757 (2009).
    Google Scholar 
    Smith, S. D., Didden-Zopfy, B. & Nobel, P. S. High-temperature responses of North American cacti. Ecology 65, 643–651 (1984).
    Google Scholar 
    Larios, E., González, E. J., Rosen, P. C., Pate, A. & Holm, P. Population projections of an endangered cactus suggest little impact of climate change. Oecologia 192, 439–448 (2020).PubMed 

    Google Scholar 
    Esparza-Olguı́n, L., Valverde, T. & Vilchis-Anaya, E. Demographic analysis of a rare columnar cactus (Neobuxbaumia macrocephala) in the Tehuacan Valley, Mexico. Biol. Conserv. 103, 349–359 (2002).
    Google Scholar 
    Seal, C. E. et al. Thermal buffering capacity of the germination phenotype across the environmental envelope of the Cactaceae. Glob. Change Biol. 23, 5309–5317 (2017).
    Google Scholar 
    Huang, J., Yu, H., Guan, X., Wang, G. & Guo, R. Accelerated dryland expansion under climate change. Nat. Clim. Change 6, 166–171 (2016).
    Google Scholar 
    Gurvich, D. E. et al. Combined effect of water potential and temperature on seed germination and seedling development of cacti from a mesic Argentine ecosystem. Flora 227, 18–24 (2017).
    Google Scholar 
    Nuzhyna, N., Baglay, K., Golubenko, A. & Lushchak, O. Anatomically distinct representatives of Cactaceae Juss. family have different response to acute heat shock stress. Flora 242, 137–145 (2018).
    Google Scholar 
    Andrade, J. L. & Nobel, P. S. Microhabitats and water relations of epiphytic cacti and ferns in a lowland neotropical forest. Biotropica 29, 261–270 (1997).
    Google Scholar 
    Williams, D. G., Hultine, K. R. & Dettman, D. L. Functional trade-offs in succulent stems predict responses to climate change in columnar cacti. J. Exp. Bot. 65, 3405–3413 (2014).PubMed 

    Google Scholar 
    Aragón-Gastélum, J. L. et al. Induced climate change impairs photosynthetic performance in Echinocactus platyacanthus, an especially protected Mexican cactus species. Flora Morphol. Distrib. Funct. Ecol. Plants 209, 499–503 (2014).
    Google Scholar 
    Martorell, C., Montañana, D. M., Ureta, C. & Mandujano, M. C. Assessing the importance of multiple threats to an endangered globose cactus in Mexico: cattle grazing, looting and climate change. Biol. Conserv. 181, 73–81 (2015).
    Google Scholar 
    Dávila, P., Téllez, O. & Lira, R. Impact of climate change on the distribution of populations of an endemic Mexican columnar cactus in the Tehuacán-Cuicatlán Valley, Mexico. Plant Biosyst. 147, 376–386 (2013).
    Google Scholar 
    Conver, J. L., Foley, T., Winkler, D. E. & Swann, D. E. Demographic changes over >70 yr in a population of saguaro cacti (Carnegiea gigantea) in the northern Sonoran Desert. J. Arid. Environ. 139, 41–48 (2017).
    Google Scholar 
    Carrillo-Angeles, I. G., Suzán-Azpiri, H., Mandujano, M. C., Golubov, J. & Martínez-Ávalos, J. G. Niche breadth and the implications of climate change in the conservation of the genus Astrophytum (Cactaceae). J. Arid. Environ. 124, 310–317 (2016).
    Google Scholar 
    de Cavalcante, A. M. B. & de Duarte, A. S. Modeling the distribution of three cactus species of the Caatinga biome in future climate scenarios. Int. J. Ecol. Environ. Sci. 45, 191–203 (2019).
    Google Scholar 
    de Cavalcante, A. M. B., de Duarte, A. S. & Ometto, J. P. H. B. Modeling the potential distribution of Epiphyllum phyllanthus (L.) Haw. under future climate scenarios in the Caatinga biome. An. Acad. Bras. Cienc. 92, 351–358 (2020).
    Google Scholar 
    Tellez-Valdes, O. & DiVila-Aranda, P. Protected areas and climate change: a case study of the cacti in the Tehuacan-Cuicatlan biosphere reserve, Mexico. Conserv. Biol. 17, 846–853 (2003).
    Google Scholar 
    dos Santos Simões, S., Zappi, D., da Costa, G. M., de Oliveira, G. & Aona, L. Y. S. Spatial niche modelling of five endemic cacti from the Brazilian Caatinga: past, present and future. Austral Ecol. 45, 1–13 (2019).
    Google Scholar 
    Gorostiague, P., Sajama, J. & Ortega-Baes, P. Will climate change cause spatial mismatch between plants and their pollinators? A test using Andean cactus species. Biol. Conserv. 226, 247–255 (2018).
    Google Scholar 
    Butler, C. J., Wheeler, E. A. & Stabler, L. B. Distribution of the threatened lace hedgehog cactus (Echinocereus reichenbachii) under various climate change scenarios. J. Torre. Bot. Soc. 139, 46–55 (2012).
    Google Scholar 
    Johnson, C. N. Species extinction and the relationship between distribution and abundance. Nature 394, 272–274 (1998).CAS 

    Google Scholar 
    Thuiller, W., Lavorel, S. & Araújo, M. B. Niche properties and geographical extent as predictors of species sensitivity to climate change. Glob. Ecol. Biogeogr. 14, 347–357 (2005).
    Google Scholar 
    Enquist, B. J. Cyberinfrastructure for an integrated botanical information network to investigate the ecological impacts of global climate change on plant biodiversity. Preprint at PeerJ https://doi.org/10.7287/peerj.preprints.2615v2 (2016).Buisson, L., Thuiller, W., Casajus, N., Lek, S. & Grenouillet, G. Uncertainty in ensemble forecasting of species distribution. Glob. Change Biol. 16, 1145–1157 (2010).
    Google Scholar 
    Thuiller, W., Guéguen, M., Renaud, J., Karger, D. N. & Zimmermann, N. E. Uncertainty in ensembles of global biodiversity scenarios. Nat. Commun. 10, 1446 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Goettsch, B., Durán, A. P. & Gaston, K. J. Global gap analysis of cactus species and priority sites for their conservation. Conserv. Biol. 33, 369–376 (2018).PubMed 

    Google Scholar 
    Maitner, B. S. et al. The bien R package: A tool to access the Botanical Information and Ecology Network (BIEN) database. Methods Ecol. Evol. 9, 373–379 (2018).
    Google Scholar 
    Karger, D. N. et al. Climatologies at high resolution for the Earth’s land surface areas. Sci. Data 4, 170122 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Sanderson, B. M., Knutti, R. & Caldwell, P. A representative democracy to reduce interdependency in a multimodel ensemble. J. Clim. 28, 5171–5194 (2015).
    Google Scholar 
    Brodzik, M. J., Billingsley, B., Haran, T., Raup, B. & Savoie, M. H. EASE-Grid 2.0: Incremental but significant improvements for Earth-gridded data sets. ISPRS Int. J. Geo-Inf. 1, 32–45 (2012).
    Google Scholar 
    Venter, O. et al. Global terrestrial human footprint maps for 1993 and 2009. Sci. Data 3, 160067 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Phillips, S. maxnet: Fitting ‘maxent’ species distribution models with ‘glmnet’. R package version 0.1.4. https://CRAN.R-project.org/package=maxnet (2017).Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Dormann, C. F. et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27–46 (2013).
    Google Scholar 
    Franklin, S. B., Gibson, D. J., Robertson, P. A., Pohlmann, J. T. & Fralish, J. S. Parallel analysis: a method for determining significant principal components. J. Veg. Sci. 6, 99–106 (1995).
    Google Scholar 
    Roberts, D. R. et al. Cross-validation strategies for data with temporal, spatial, hierarchical, or phylogenetic structure. Ecography 40, 913–929 (2017).
    Google Scholar 
    Merow, C., Smith, M. J. & Silander, J. A. A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36, 1058–1069 (2013).
    Google Scholar 
    Allouche, O., Tsoar, A. & Kadmon, R. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43, 1223–1232 (2006).
    Google Scholar 
    Calabrese, J. M., Certain, G., Kraan, C. & Dormann, C. F. Stacking species distribution models and adjusting bias by linking them to macroecological models. Glob. Ecol. Biogeogr. 23, 99–112 (2014).
    Google Scholar 
    R Core Team R: A Language and Environment for Statistical Computing Version 3.6.0 (R Foundation for Statistical Computing, 2019). https://www.R-project.org/ More