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    Stable isotopes unveil one millennium of domestic cat paleoecology in Europe

    Turner, D. & Bateson, P. (eds) The Domestic Cat: The Biology of Its Behaviour (Cambridge Univ. Press, 2000).
    Google Scholar 
    Bradshaw, J. W. S., Goodwin, D., Legrand-Defrétin, V. & Nott, H. M. R. Food selection by the domestic cat, an obligate carnivore. Comp. Biochem. Physiol. A Physiol. 114, 205–209 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    Trouwborst, A., McCormack, P. C. & Martínez Camacho, E. Domestic cats and their impacts on biodiversity: A blind spot in the application of nature conservation law. People Nat. 2, 235–250 (2020).Article 

    Google Scholar 
    Crowley, S. L., Cecchetti, M. & McDonald, R. A. Our wild companions: Domestic cats in the anthropocene. Trends Ecol. Evol. 35, 477–483 (2020).PubMed 
    Article 

    Google Scholar 
    Driscoll, C. A. et al. The Near Eastern origin of cat domestication. Science 317, 519–523 (2007).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Van Neer, W., Linseele, V., Friedman, R. & De Cupere, B. More evidence for cat taming at the Predynastic elite cemetery of Hierakonpolis (Upper Egypt). J. Archaeol. Sci. 45, 103–111 (2014).Article 

    Google Scholar 
    Ottoni, C. et al. The palaeogenetics of cat dispersal in the ancient world. Nat. Ecol. Evol. 1, 0139 (2017).Article 

    Google Scholar 
    Baca, M. et al. Human-mediated dispersal of cats in the Neolithic Central Europe. Heredity 121, 557–563 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Vigne, J. The beginning of cat domestication in East and West Asia. Doc. Archaeobiol. 15, 343–354 (2019).
    Google Scholar 
    Krajcarz, M. et al. Ancestors of domestic cats in Neolithic Central Europe: Isotopic evidence of a synanthropic diet. Proc. Natl. Acad. Sci. USA 117, 17710–17719 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Piontek, A. M. et al. Analysis of cat diet across an urbanisation gradient. Urban Ecosyst. 24, 59–69 (2021).Article 

    Google Scholar 
    Medina, F. M. et al. A global review of the impacts of invasive cats on island endangered vertebrates. Glob. Chang. Biol. 17, 3503–3510 (2011).ADS 
    Article 

    Google Scholar 
    Moseby, K. E., Peacock, D. E. & Read, J. L. Catastrophic cat predation: A call for predator profiling in wildlife protection programs. Biol. Conserv. 191, 331–340 (2015).Article 

    Google Scholar 
    Loss, S. R., Will, T. & Marra, P. P. The impact of free-ranging domestic cats on wildlife of the United States. Nat. Commun. 4, 1396 (2013).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Beaumont, M. et al. Genetic diversity and introgression in the Scottish wildcat. Mol. Ecol. 10, 319–336 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Beugin, M. P. et al. Hybridization between Felis silvestris silvestris and Felis silvestris catus in two contrasted environments in France. Ecol. Evol. 10, 263–276 (2020).PubMed 
    Article 

    Google Scholar 
    Biró, Z., Lanszki, J., Szemethy, L., Heltai, M. & Randi, E. Feeding habits of feral domestic cats (Felis catus), wild cats (Felis silvestris) and their hybrids: Trophic niche overlap among cat groups in Hungary. J. Zool. 266, 187–196 (2005).Article 

    Google Scholar 
    Széles, G. L., Purger, J. J., Molnár, T. & Lanszki, J. Comparative analysis of the diet of feral and house cats and wildcat in Europe. Mammal. Res. 63, 43–53 (2018).Article 

    Google Scholar 
    Ottoni, C. & Van Neer, W. The dispersal of the domestic cat paleogenetic and zooarcheological evidence. Near East. Archaeol. 83, 38–45 (2020).Article 

    Google Scholar 
    Bitz-Thorsen, J. & Gotfredsen, A. B. Domestic cats (Felis catus) in Denmark have increased significantly in size since the Viking Age. Danish J. Archaeol. 7, 241–254 (2018).Article 

    Google Scholar 
    Faure, E. & Kitchener, A. C. An archaeological and historical review of the relationships between felids and people. Anthrozoos 22, 221–238 (2009).Article 

    Google Scholar 
    von den Driesch, A. Kulturgeschichte der Hauskatze. In Krankheiten der Katze, Bd. 1 (eds Schmidt, V. & Horzinek, M. C.) 17–40 (Fischer, 1992).
    Google Scholar 
    Głażewska, I. & Kijewski, T. A new view on the European feline population from mtDNA analysis in Polish domestic cats. Forensic Sci. Int. Genet. 27, 116–122 (2017).PubMed 
    Article 
    CAS 

    Google Scholar 
    Cucchi, T. et al. Tracking the Near Eastern origins and European dispersal of the western house mouse. Sci. Rep. 10, 8276 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Van Klinken, G. J., Richards, M. P. & Hedges, B. E. M. An overview of causes for stable isotopic variations in past European human populations: environmental, ecophysiological, and cultural effects. In Biogeochemical Approaches to Paleodietary Analysis (eds Ambrose, S. & Katzenberg, M.) 39–63 (Kluwer Academic Publishers, 2002). https://doi.org/10.1007/0-306-47194-9_3.Chapter 

    Google Scholar 
    Drucker, D. G., Bridault, A., Hobson, K. A., Szuma, E. & Bocherens, H. Can carbon-13 in large herbivores reflect the canopy effect in temperate and boreal ecosystems? Evidence from modern and ancient ungulates. Palaeogeogr. Palaeoclimatol. Palaeoecol. 266, 69–82 (2008).Article 

    Google Scholar 
    Koch, P. L. Isotopic study of the biology of modern and fossil vertebrates. In Stable Isotopes in Ecology and Environmental Science (eds Michener, R. & Lajtha, K.) 99–154 (Blackwell Publishing Ltd, 2007). https://doi.org/10.1002/9780470691854.ch5.Chapter 

    Google Scholar 
    Hofman-Kamińska, E. et al. Foraging habitats and niche partitioning of European large herbivores during the holocene—Insights from 3D dental microwear texture analysis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 506, 183–195 (2018).Article 

    Google Scholar 
    Bocherens, H., Hofman-Kamińska, E., Drucker, D. G., Schmölcke, U. & Kowalczyk, R. European bison as a refugee species? Evidence from isotopic data on Early Holocene bison and other large herbivores in northern Europe. PLoS ONE 10, 1–19 (2015).Article 
    CAS 

    Google Scholar 
    Hu, Y. et al. Earliest evidence for commensal processes of cat domestication. Proc. Natl. Acad. Sci. USA. 111, 116–120 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Haruda, A. F. et al. The earliest domestic cat on the Silk Road. Sci. Rep. 10, 11241 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Meckstroth, A. M., Miles, A. K. & Chandra, S. Diets of introduced predators using stable isotopes and stomach contents. J. Wildl. Manag. 71, 2387–2392 (2007).Article 

    Google Scholar 
    McDonald, B. W. et al. High variability within pet foods prevents the identification of native species in pet cats’ diets using isotopic evaluation. PeerJ 8, e8337 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Maeda, T., Nakashita, R., Shionosaki, K., Yamada, F. & Watari, Y. Predation on endangered species by human-subsidized domestic cats on Tokunoshima Island. Sci. Rep. 9, 16200 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Stewart, G. R., Aidar, M. P. M., Joly, C. A. & Schmidt, S. Impact of point source pollution on nitrogen isotope signatures (δ15N) of vegetation in SE Brazil. Oecologia 131, 468–472 (2002).ADS 
    PubMed 
    Article 

    Google Scholar 
    Graven, H., Keeling, R. F. & Rogelj, J. Changes to carbon isotopes in atmospheric CO2 over the industrial era and into the future. Glob. Biogeochem. Cycles 34, 1–21 (2020).Article 
    CAS 

    Google Scholar 
    DeNiro, M. J. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317, 806–809 (1985).ADS 
    CAS 
    Article 

    Google Scholar 
    Linderholm, A. & Kjellström, A. Stable isotope analysis of a medieval skeletal sample indicative of systemic disease from Sigtuna Sweden. J. Archaeol. Sci. 38, 925–933 (2011).Article 

    Google Scholar 
    Webb, E. C. et al. Compound-specific amino acid isotopic proxies for distinguishing between terrestrial and aquatic resource consumption. Archaeol. Anthropol. Sci. 10, 1–18 (2018).Article 

    Google Scholar 
    Müldner, G. & Richards, M. P. Stable isotope evidence for 1500 years of human diet at the city of York, UK. Am. J. Phys. Anthropol. 133, 682–697 (2007).PubMed 
    Article 

    Google Scholar 
    Müldner, G. & Richards, M. P. Fast or feast: Reconstructing diet in later medieval England by stable isotope analysis. J. Archaeol. Sci. 32, 39–48 (2005).Article 

    Google Scholar 
    van der Sluis, L. G., Hollund, H. I., Kars, H., Sandvik, P. U. & Denham, S. D. A palaeodietary investigation of a multi-period churchyard in Stavanger, Norway, using stable isotope analysis (C, N, H, S) on bone collagen. J. Archaeol. Sci. Rep. 9, 120–133 (2016).
    Google Scholar 
    Polet, C. & Katzenberg, M. A. Reconstruction of the diet in a mediaeval monastic community from the coast of Belgium. J. Archaeol. Sci. 30, 525–533 (2003).Article 

    Google Scholar 
    Kosiba, S. B., Tykot, R. H. & Carlsson, D. Stable isotopes as indicators of change in the food procurement and food preference of Viking Age and Early Christian populations on Gotland (Sweden). J. Anthropol. Archaeol. 26, 394–411 (2007).Article 

    Google Scholar 
    Olsen, K. C. et al. Isotopic anthropology of rural German medieval diet: Intra- and inter-population variability. Archaeol. Anthropol. Sci. 10, 1053–1065 (2018).Article 

    Google Scholar 
    Benevolo, L. The European City (Blackwell Publishers, 1993).
    Google Scholar 
    Barrett, J. et al. Detecting the medieval cod trade: A new method and first results. J. Archaeol. Sci. 35, 850–861 (2008).Article 

    Google Scholar 
    Barrett, J. H. et al. Interpreting the expansion of sea fishing in medieval Europe using stable isotope analysis of archaeological cod bones. J. Archaeol. Sci. 38, 1516–1524 (2011).Article 

    Google Scholar 
    Bogaard, A., Heaton, T. H. E., Poulton, P. & Merbach, I. The impact of manuring on nitrogen isotope ratios in cereals: Archaeological implications for reconstruction of diet and crop management practices. J. Archaeol. Sci. 34, 335–343 (2007).Article 

    Google Scholar 
    Heaton, T. H. E. Spatial, species, and temporal variations in the 13C/12C ratios of C3 plants: Implications for palaeodiet studies. J. Archaeol. Sci. 26, 637–649 (1999).Article 

    Google Scholar 
    Bogaard, A. et al. Crop manuring and intensive land management by Europe’s first farmers. Proc. Natl. Acad. Sci. USA. 110, 12589–12594 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Styring, A. K. et al. Refining human palaeodietary reconstruction using amino acid δ15N values of plants, animals and humans. J. Archaeol. Sci. 53, 504–515 (2015).CAS 
    Article 

    Google Scholar 
    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 
    Fuller, B. T., Müldner, G., Van Neer, W., Ervynck, A. & Richards, M. P. Carbon and nitrogen stable isotope ratio analysis of freshwater, brackish and marine fish from Belgian archaeological sites (1st and 2nd millennium AD). J. Anal. At. Spectrom. 27, 807–820 (2012).CAS 
    Article 

    Google Scholar 
    Robson, H. K. et al. Carbon and nitrogen stable isotope values in freshwater, brackish and marine fish bone collagen from Mesolithic and Neolithic sites in central and northern Europe. Environ. Archaeol. 21, 105–118 (2016).Article 

    Google Scholar 
    Hobson, K. A., Piatt, J. F. & Pitocchelli, J. Using stable isotopes to determine seabird trophic relationships. J. Anim. Ecol. 63, 786–798 (1994).Article 

    Google Scholar 
    Guiry, E. & Buckley, M. Urban rats have less variable, higher protein diets. Proc. R. Soc. B Biol. Sci. 285, 20181441 (2018).Article 
    CAS 

    Google Scholar 
    Bicknell, A. W. J. et al. Stable isotopes reveal the importance of seabirds and marine foods in the diet of St Kilda field mice. Sci. Rep. 10, 1–12 (2020).Article 
    CAS 

    Google Scholar 
    Hoffmann, R. C. Medieval fishing. In Working with Water in Medieval Europe. Technology and Resource-Use (ed. Squatriti, P.) 331–393 (Brill, 2000).
    Google Scholar 
    Gillies, C. & Clout, M. The prey of domestic cats (Felis catus) in two suburbs of Auckland City, New Zealand. J. Zool. 259, 309–315 (2003).Article 

    Google Scholar 
    Brickner-Braun, I., Geffen, E. & Yom-Tov, Y. The domestic cat as a predator of Israeli wildlife. Isr. J. Ecol. Evol. 53, 129–142 (2007).Article 

    Google Scholar 
    Flockhart, D. T. T., Norris, D. R. & Coe, J. B. Predicting free-roaming cat population densities in urban areas. Anim. Conserv. 19, 472–483 (2016).Article 

    Google Scholar 
    Castañeda, I., Zarzoso-Lacoste, D. & Bonnaud, E. Feeding behaviour of red fox and domestic cat populations in suburban areas in the south of Paris. Urban Ecosyst. 23, 731–743 (2020).Article 

    Google Scholar 
    Zhu, Y., Siegwolf, R. T. W., Durka, W. & Körner, C. Phylogenetically balanced evidence for structural and carbon isotope responses in plants along elevational gradients. Oecologia 162, 853–863 (2010).ADS 
    PubMed 
    Article 

    Google Scholar 
    Männel, T. T., Auerswald, K. & Schnyder, H. Altitudinal gradients of grassland carbon and nitrogen isotope composition are recorded in the hair of grazers. Glob. Ecol. Biogeogr. 16, 583–592 (2007).Article 

    Google Scholar 
    Pińska, K. & Badura, M. Warunki przyrodnicze i dieta roślinna mieszkańców Pucka w późnym średniowieczu. In Puck – kultura materialna małego miasta w późnym średniowieczu (ed. Starski, M.) 517 (Uniwersytet Warszawski, 2017).
    Google Scholar 
    Lefebvre, A. et al. Morphology of estuarine bedforms, Weser Estuary, Germany. Earth Surf. Process. Landforms 47, 242–256 (2022).ADS 
    Article 

    Google Scholar 
    Bischop, D. & Von der Küchelmann, H. C. Küche in den Graben – Bremens Stadtgraben und die Essgewohnheiten seiner Anwohner an der Wende zur Frühen Neuzeit. In Lebensmittel im Mittelalter und in der frühen Neuzeit. Erzeugung, Verarbeitung, Versorgung. Beiträge des 16. Kolloquiums des Arbeitskreises zur archäologischen Erforschung des mittelalterlichen Handwerks, Soester Beiträge zur Archäologie 15 (ed. Melzer, W.) 137–151 (Mocker und Jahn, 2018).
    Google Scholar 
    Elmshäuser, K. & Pordzik, V. V. Lachsgarnen, Tomen und Kumpanen – Die älteste Bremer Fischeramtsrolle. Bremisches Jahrb. 98, 13–72 (2019).
    Google Scholar 
    Küchelmann, H. C. Viel Butter bei wenig Fisch. Zwei Fischknochenkomplexe des 12.–13. Jahrhunderts aus der Bremer Altstadt. In Grenzen überwinden. Archäologie zwischen Disziplin und Disziplinen. Festschrift für Uta Halle zum 65. Geburtstag, Internationale Archäologie Studia Honoraria 40 (eds Kahlow, S. et al.) 413–426 (Verlag Marie Leidorf GmbH, 2021).
    Google Scholar 
    Schwarcz, H. P. & Schoeninger, M. J. Stable isotope analyses in human nutritional ecology. Am. J. Phys. Anthropol. 34, 283–321 (1991).Article 

    Google Scholar 
    Wallace, M. et al. Stable carbon isotope analysis as a direct means of inferring crop water status and water management practices. World Archaeol. 45, 388–409 (2013).Article 

    Google Scholar 
    van der Merwe, N. J. & Medina, E. The canopy effect, carbon isotope ratios and foodwebs in amazonia. J. Archaeol. Sci. 18, 249–259 (1991).Article 

    Google Scholar 
    Ervynck, A. Orant, pugnant, laborant. The diet of the three orders in the feudal society of medieval north-western Europe. In Behaviour Behind Bones. The Zooarchaeology of Ritual, Religion, Status and Identity (eds O’Day, S. J. et al.) 215–223 (Oxbow Books, 2004).
    Google Scholar 
    von den Driesch, A. A guide to the measurement of animal bones from archaeological sites. Peabody Museum Bull. 1, 1–137 (1976).
    Google Scholar 
    O’Connor, T. P. Wild or domestic? Biometric variation in the cat Felis silvestris Schreber. Int. J. Osteoarchaeol. 17, 581–595 (2007).Article 

    Google Scholar 
    Kratochvíl, Z. Schadelkriterien der Wild- und Hauskatze (Felis silvestris silvestris Schreber 1777 und Felis s. f. catus L. 1758). Acta Sci. Nat. Brno 7, 1–50 (1973).
    Google Scholar 
    Kratochvíl, Z. Das Postkranialskelett der Wild- und Hauskatze (Felis silvestris und F. lybica f. catus). Acta Sci. Nat. Brno 10, 1–43 (1976).
    Google Scholar 
    Dyce, K. M., Sack, W. O. & Wensing, C. J. G. Textbook of Veterinary Anatomy (Saunders/Elsevier, 2010).
    Google Scholar 
    Krajcarz, M. et al. On the trail of the oldest domestic cat in Poland. An insight from morphometry, ancient DNA and radiocarbon dating. Int. J. Osteoarchaeol. 26, 912–919 (2016).Article 

    Google Scholar 
    Bronk Ramsey, C. Radiocarbon calibration and analysis of stratigraphy: The OxCal program. Radiocarbon 37, 425–430 (1995).CAS 
    Article 

    Google Scholar 
    Bronk Ramsey, C., Dee, M., Lee, S., Nakagawa, T. & Staff, R. Developments in the calibration and modeling of radiocarbon dates. Radiocarbon 52, 953–961 (2010).Article 

    Google Scholar 
    Ferreira, J. P., Leitão, I., Santos-Reis, M. & Revilla, E. Human-related factors regulate the spatial ecology of domestic cats in sensitive areas for conservation. PLoS ONE 6, e25970 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pirie, T. J., Thomas, R. L. & Fellowes, M. D. E. Pet cats (Felis catus) from urban boundaries use different habitats, have larger home ranges and kill more prey than cats from the suburbs. Landsc. Urban Plan. 220, 104338 (2022).Article 

    Google Scholar 
    Bocherens, H. et al. Paleobiological implications of the isotopic signatures (13C, 15N) of fossil mammal collagen in Scladina cave (Sclayn, Belgium). Quat. Res. 48, 370–380 (1997).Article 

    Google Scholar 
    Longin, R. New method of collagen extraction for radiocarbon dating. Nature 230, 241–242 (1971).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Boudin, M., Boeckx, P., Vandenabeele, P. & Van Strydonck, M. Improved radiocarbon dating of contaminated protein-containing archaeological samples via cross-flow nanofiltrated amino acids. Rapid Commun. Mass Spectrom. 27, 2039–2050 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Wojcieszak, M., Van Den Brande, T., Ligovich, G. & Boudin, M. Pretreatment protocols performed at the Royal Institute for Cultural Heritage (RICH) prior to AMS 14C measurements. Radiocarbon 62, e14–e24 (2020).Article 

    Google Scholar 
    Hammer, Ø. PAST. PAleontological Statistics. Version 4.05 Reference manual (Natural History Museum University of Oslo, 2021).
    Google Scholar 
    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).
    Google Scholar 
    Rohland, N., Glocke, I., Aximu-Petri, A. & Meyer, M. Extraction of highly degraded DNA from ancient bones, teeth and sediments for high-throughput sequencing. Nat. Protoc. 13, 2447–2461 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nguyen, L. T., Schmidt, H. A., Von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    Using metabarcoding and droplet digital PCR to investigate drivers of historical shifts in cyanobacteria from six contrasting lakes

    Paerl, H. W. & Huisman, J. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1, 27–37 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Paerl, H. W. & Paul, V. J. Climate change: links to global expansion of harmful cyanobacteria. Water Res. 46, 1349–1363 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Huisman, J. et al. Cyanobacterial blooms. Nat. Rev. Microbiol. 16, 471 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Reissig, M., Trochine, C., Queimaliños, C., Balseiro, E. & Modenutti, B. Impact of fish introduction on planktonic food webs in lakes of the Patagonian Plateau. Biol. Conserv. 132, 437–447 (2006).Article 

    Google Scholar 
    Britton, J. R., Davies, G. D. & Harrod, C. Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK. Biol. Invasions 12, 1533–1542 (2010).Article 

    Google Scholar 
    Beaulieu, M., Pick, F. & Gregory-Eaves, I. Nutrients and water temperature are significant predictors of cyanobacterial biomass in a 1147 lakes data set. Limnol. Oceanogr. 58, 1736–1746 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    O’Neil, J. M., Davis, T. W., Burford, M. A. & Gobler, C. J. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14, 313–334 (2012).Article 
    CAS 

    Google Scholar 
    Paerl, H. W. & Huisman, J. Blooms like it hot. Science 320, 57–58 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring, and Management. (E & FN Spon, 1999).Sukenik, A., Quesada, A. & Salmaso, N. Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers. Conserv. 24, 889–908 (2015).Article 

    Google Scholar 
    Ibelings, B. W., Bormans, M., Fastner, J. & Visser, P. M. CYANOCOST special issue on cyanobacterial blooms: synopsis—a critical review of the management options for their prevention, control and mitigation. Aquat. Ecol. 50, 595–605 (2016).CAS 
    Article 

    Google Scholar 
    Paerl, H. W. Mitigating harmful cyanobacterial blooms in a human- and climatically-impacted world. Life 4, 988–1012 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rastogi, R. P., Madamwar, D. & Incharoensakdi, A. Bloom dynamics of cyanobacteria and their toxins: environmental health impacts and mitigation strategies. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.01254 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ewing, H. A. et al. “New” cyanobacterial blooms are not new: two centuries of lake production are related to ice cover and land use. Ecosphere 11, e03170 (2020).Article 

    Google Scholar 
    McGlone, M. S. & Wilmshurst, J. M. Dating initial Maori environmental impact in New Zealand. Quat. Int. 59, 5–16 (1999).Article 

    Google Scholar 
    Brooking, A. P. D. of H. T. & Brooking, T. The History of New Zealand. (Greenwood Publishing Group, 2004).Wilmshurst, J. M., Anderson, A. J., Higham, T. F. G. & Worthy, T. H. Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat. PNAS 105, 7676–7680 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McGlone, M. S. The Polynesian settlement of New Zealand in relation to environmental and biotic changes. N. Z. J. Ecol. 12, 115–129 (1989).
    Google Scholar 
    McGlone, M. S. Polynesian deforestation of New Zealand: a preliminary synthesis. Archaeol. Ocean. 18, 11–25 (1983).Article 

    Google Scholar 
    McWethy, D. B. et al. Rapid landscape transformation in South Island, New Zealand, following initial Polynesian settlement. PNAS 107, 21343–21348 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McWethy, D. B., Wilmshurst, J. M., Whitlock, C., Wood, J. R. & McGlone, M. S. A high-resolution chronology of rapid forest transitions following Polynesian arrival in New Zealand. PLoS ONE 9, e111328 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Star, P. New Zealand environmental history: a question of attitudes. Environ. Hist. Camb. 9, 463–475 (2003).Article 

    Google Scholar 
    Clark, A. H. The Invasion of New Zealand by Plants, People, and Animals (Rutgers University Press, 1949).
    Google Scholar 
    Wilmshurst, J. M. Human effects on the environment: European impact. Te Ara: The Encyclopedia of New Zealand https://teara.govt.nz/en/human-effects-on-the-environment/page-3 (2007).Smol, J. P. The ratio of diatom frustules to chrysophycean statospores: a useful paleolimnological index. Hydrobiologia 123, 199–208 (1985).Article 

    Google Scholar 
    Rees, A. B. H., Cwynar, L. C. & Cranston, P. S. Midges (Chironomidae, Ceratopogonidae, Chaoboridae) as a temperature proxy: a training set from Tasmania, Australia. J. Paleolimnol. 40, 1159–1178 (2008).ADS 
    Article 

    Google Scholar 
    Epp, L. S., Stoof, K. R., Trauth, M. H. & Tiedemann, R. Historical genetics on a sediment core from a Kenyan lake: intraspecific genotype turnover in a tropical rotifer is related to past environmental changes. J. Paleolimnol. 43, 939–954 (2010).ADS 
    Article 

    Google Scholar 
    Buchaca, T. et al. Rapid ecological shift following piscivorous fish introduction to increasingly eutrophic and warmer Lake Furnas (Azores Archipelago, Portugal): a paleoecological approach. Ecosystems 14, 458–477 (2011).CAS 
    Article 

    Google Scholar 
    Cristescu, M. E. & Hebert, P. D. N. Uses and misuses of environmental DNA in biodiversity science and conservation. Annu. Rev. Ecol. Evol. Syst. 49, 209–230 (2018).Article 

    Google Scholar 
    Giguet-Covex, C. et al. Long livestock farming history and human landscape shaping revealed by lake sediment DNA. Nat. Commun. 5, 3211 (2014).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    Alsos, I. G. et al. Plant DNA metabarcoding of lake sediments: how does it represent the contemporary vegetation. PLoS ONE 13, e0195403 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Nelson-Chorney, H. T. et al. Environmental DNA in lake sediment reveals biogeography of native genetic diversity. Front. Ecol. Environ. 17, 313–318 (2019).
    Google Scholar 
    Capo, E. et al. Lake sedimentary DNA research on past terrestrial and aquatic biodiversity: overview and recommendations. Quaternary 4, 6 (2021).Article 

    Google Scholar 
    Shokralla, S., Spall, J. L., Gibson, J. F. & Hajibabaei, M. Next-generation sequencing technologies for environmental DNA research. Mol. Ecol. 21, 1794–1805 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C. & Willerslev, E. Towards next-generation biodiversity assessment using DNA metabarcoding. Mol. Ecol. 21, 2045–2050 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Thomsen, P. F. & Willerslev, E. Environmental DNA: an emerging tool in conservation for monitoring past and present biodiversity. Biol. Conserv. 183, 4–18 (2015).Article 

    Google Scholar 
    Keeley, N., Wood, S. A. & Pochon, X. Development and preliminary validation of a multi-trophic metabarcoding biotic index for monitoring benthic organic enrichment. Ecol. Ind. 85, 1044–1057 (2018).CAS 
    Article 

    Google Scholar 
    Monchamp, M.-E., Walser, J.-C., Pomati, F. & Spaak, P. Sedimentary DNA reveals cyanobacterial community diversity over 200 years in two perialpine lakes. Appl. Environ. Microbiol. 82, 6472–6482 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pal, S., Gregory-Eaves, I. & Pick, F. R. Temporal trends in cyanobacteria revealed through DNA and pigment analyses of temperate lake sediment cores. J. Paleolimnol. 54, 87–101 (2015).ADS 
    Article 

    Google Scholar 
    Dodsworth, W. Temporal Trends in Cyanobacteria Through Paleo-Genetic Analyses. (Université d’Ottawa/University of Ottawa, 2020). https://doi.org/10.20381/ruor-24401.Rinta-Kanto, J. M. et al. The diversity and distribution of toxigenic Microcystis spp. in present day and archived pelagic and sediment samples from Lake Erie. Harmful Algae 8, 385–394 (2009).CAS 
    Article 

    Google Scholar 
    Zastepa, A. et al. Reconstructing a long-term record of microcystins from the analysis of lake sediments. Sci. Total Environ. 579, 893–901 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Schallenberg, M. et al. Ecosystem services of lakes. In Ecosystem Services in New Zealand (ed. Dymond, J.) 23 (Manaaki Whenua Press, 2013).
    Google Scholar 
    Ministry for the Environment & Ausseil, A.-G. Our freshwater 2020. www.mfe.govt.nz (2020).Takiwa—Map Page. https://lernz.takiwa.co/map.Leathwick, J. et al. Freshwater ecosystems of New Zealand (FENZ) geodatabase. Users guide. (2010).Cochrane, L. Reconstructing Ecological Change, Catchment Disturbance, and Anthropogenic Impact over the last 3000 years at Lake Pounui, Wairarapa, New Zealand. (2017).Burns, C. W. & Mitchell, S. F. Seasonal succession and vertical distribution of phytoplankton in Lake Hayes and Lake Johnson, South Island, New Zealand. N. Z. J. Mar. Freshw. Res. 8, 167–209 (1974).Article 

    Google Scholar 
    Lawa. Land, Air, Water Aotearoa (LAWA) https://www.lawa.org.nz/ (2018).Bunny, T., Perrie, A., Milne, J. & Keenan, L. Lake water quality in the Ruamāhanga Whaitua. 17 (2014).McKinnon, M. Volcanic Plateau region: The lure of trout. Te Ara—The Encyclopedia of New Zealand https://teara.govt.nz/en/volcanic-plateau-region/page-8 (2015).Burns, C. W. & Mitchell, S. F. Seasonal succession and vertical distribution of zooplankton in Lake Hayes and Lake Johnson. N. Z. J. Mar. Freshw. Res. 14, 189–204 (1980).Article 

    Google Scholar 
    Schallenberg, M. & Schallenberg, L. Lake Hayes restoration and monitoring plan. 55 https://a234f952-dbf2-444e-983e-ef311d984ee7.filesusr.com/ugd/c1b10b_d2993ed023cd4bdbac7eef71a89c2de7.pdf (2017).NIWA. NIWA https://niwa.co.nz/.Mackereth, F. J. H. A portable core sampler for lake deposits. Limnol. Oceanogr. 3, 181–191 (1958).ADS 
    Article 

    Google Scholar 
    Howarth, J. D., Fitzsimons, S. J., Norris, R. J. & Jacobsen, G. E. Lake sediments record cycles of sediment flux driven by large earthquakes on the Alpine fault, New Zealand. Geology 40, 1091–1094 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    Trodahl, M. I., Rees, A. B. H., Newnham, R. M. & Vandergoes, M. J. Late Holocene geomorphic history of Lake Wairarapa, North Island, New Zealand. N. Z. J. Geol. Geophys. 59, 330–340 (2016).CAS 
    Article 

    Google Scholar 
    Khan, S., Puddick, J., Burns, C. W., Closs, G. & Schallenberg, M. Palaeolimnological evaluation of historical nutrient and food web contributions to the eutrophication of two monomictic lakes. Submitted for Journal Publication (2022).Rinta-Kanto, J. M. et al. Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in Western Lake Erie using quantitative real-time PCR. Environ. Sci. Technol. 39, 4198–4205 (2005).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Nübel, U., Garcia-Pichel, F. & Muyzer, G. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl. Environ. Microbiol. 63, 3327–3332 (1997).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020).RStudio Team. RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. (2020).Wickham, H. et al. Welcome to the Tidyverse. J. Open Sour. Softw. 4, 1686 (2019).ADS 
    Article 

    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).MATH 
    Book 

    Google Scholar 
    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12 (2011).Article 

    Google Scholar 
    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    Yilmaz, P. et al. The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42, D643–D648 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Glöckner, F. O. et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J. Biotechnol. 261, 169–176 (2017).PubMed 
    Article 
    CAS 

    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: an R Package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5–6. 2019. (2019).Williams, P. A. & Cameron, E. K. Creating gardens: the diversity and progression of European plant introductions. In Biological Invasions in New Zealand Vol. 186 (eds Allen, R. B. & Lee, W. G.) 33–47 (Springer-Verlag, 2006).Chapter 

    Google Scholar 
    Simpson, G. L. Modelling palaeoecological time series using generalised additive models. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2018.00149 (2018).Article 

    Google Scholar 
    Chen, H. & Boutros, P. C. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinform. 12, 35 (2011).Article 

    Google Scholar 
    Juggins, S. rioja: analysis of quaternary science data. (2020).de Vries, A. & Ripley, B. D. ggdendro: create dendrograms and tree diagrams using ‘ggplot2’. (2022).Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).
    Google Scholar 
    Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253 (2006).MathSciNet 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    Soo, R. M. et al. An expanded genomic representation of the phylum Cyanobacteria. Genome Biol. Evol. 6, 1031–1045 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    MacKeigan, P. W. et al. Comparing microscopy and DNA metabarcoding techniques for identifying cyanobacteria assemblages across hundreds of lakes. Harmful Algae 113, 102187 (2022).CAS 
    PubMed 
    Article 

    Google Scholar 
    Wood, S. A. et al. Trophic state and geographic gradients influence planktonic cyanobacterial diversity and distribution in New Zealand lakes. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiw234 (2017).Article 
    PubMed 

    Google Scholar 
    Becker, S., Richl, P. & Ernst, A. Seasonal and habitat-related distribution pattern of Synechococcus genotypes in Lake Constance. FEMS Microbiol. Ecol. 62, 64–77 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sánchez-Baracaldo, P., Handley, B. A. & Hayes, P. K. Picocyanobacterial community structure of freshwater lakes and the Baltic Sea revealed by phylogenetic analyses and clade-specific quantitative PCR. Microbiology (Reading) 154, 3347–3357 (2008).Article 
    CAS 

    Google Scholar 
    Pilon, S. et al. Contrasting histories of microcystin-producing cyanobacteria in two temperate lakes as inferred from quantitative sediment DNA analyses. Lake Reserv. Manag. 35, 102–117 (2019).CAS 
    Article 

    Google Scholar 
    Queenstown’s Pioneering Beginnings. https://www.queenstownnz.co.nz/stories/post/queenstowns-pioneer-beginnings/ (2017).Fish, G. R. A limnological study of four lakes near Rotorua. N. Z. J. Mar. Freshw. Res. 4, 165–194 (1970).Article 

    Google Scholar 
    Lake Rotoehu—Lakes Water Quality Society. https://lakeswaterquality.co.nz/lake-rotoehu/.Bay of Plenty Regional Council, Rotorua District Council, & Te Arawa Lakes Trust. Lake Rotoehu Action Plan. 61 http://www.rotorualakes.co.nz/vdb/document/76 (2007).Hobbs, W. O. et al. Using a lake sediment record to infer the long-term history of cyanobacteria and the recent rise of an anatoxin producing Dolichospermum sp.. Harmful Algae 101, 101971 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    de la Escalera, G. M., Antoniades, D., Bonilla, S. & Piccini, C. Application of ancient DNA to the reconstruction of past microbial assemblages and for the detection of toxic cyanobacteria in subtropical freshwater ecosystems. Mol. Ecol. 23, 5791–5802 (2014).Article 
    CAS 

    Google Scholar 
    Retrolens—Historical Imagery Resource. https://retrolens.co.nz/.Strayer, D. L. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshw. Biol. 55, 152–174 (2010).Article 

    Google Scholar 
    Hall, S. R. & Mills, E. L. Exotic species in large lakes of the world. Aquat. Ecosyst. Health Manag. 3, 105–135 (2000).Article 

    Google Scholar 
    Gehrke, P. C. & Harris, J. H. The role of fish in cyanobacterial blooms in Australia. Mar. Freshw. Res. 45, 905–915 (1994).Article 

    Google Scholar 
    Burns, C. W. & Schallenberg, M. Impacts of nutrients and zooplankton on the microbial food web of an ultra-oligotrophic lake. J. Plankton Res. 20, 1501–1525 (1998).Article 

    Google Scholar 
    Rowe, D. K. & Schallenberg, M. Food webs in lakes. In Freshwaters of New Zealand (ed. Harding, J. S.) 23 (Wellington, N.Z.: New Zealand Hydrological Society, 2004).Gliwicz, Z. M. & Pijanowska, J. The role of predation in zooplankton succession. In Plankton Ecology: Succession in Plankton Communities (ed. Sommer, U.) 253–296 (Springer, 1989).Chapter 

    Google Scholar 
    Vanni, M. J. & Findlay, D. L. Trophic cascades and phytoplankton community structure. Ecology 71, 921–937 (1990).Article 

    Google Scholar 
    Smith, K. F. & Lester, P. J. Trophic interactions promote dominance by cyanobacteria (Anabaena spp.) in the pelagic zone of lower Karori reservoir, Wellington, New Zealand. N. Z. J. Mar. Freshw. Res. 41, 143–155 (2007).Article 

    Google Scholar 
    Smith, K. F. & Lester, P. J. Cyanobacterial blooms appear to be driven by top-down rather than bottom-up effects in the Lower Karori Reservoir (Wellington, New Zealand). N. Z. J. Mar. Freshw. Res. 40, 53–63 (2006).CAS 
    Article 

    Google Scholar 
    Caroppo, C. Ecology and biodiversity of picoplanktonic cyanobacteria in coastal and brackish environments. Biodivers. Conserv. 24, 949–971 (2015).Article 

    Google Scholar 
    Pulina, S. et al. Picophytoplankton seasonal dynamics and interactions with environmental variables in three Mediterranean coastal lagoons. Estuaries Coasts 40, 469–478 (2017).CAS 
    Article 

    Google Scholar 
    Callieri, C. Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshw. Rev. 1, 1–28 (2008).Article 

    Google Scholar 
    Keefer, D. K. Investigating landslides caused by earthquakes: a historical review. Surv. Geophys. 23, 473–510 (2002).ADS 
    Article 

    Google Scholar 
    Fan, X. et al. Earthquake-induced chains of geologic hazards: patterns, mechanisms, and impacts. Rev. Geophys. 57, 421–503 (2019).ADS 
    Article 

    Google Scholar 
    Manighetti, I. et al. Repeated giant earthquakes on the Wairarapa fault, New Zealand, revealed by Lidar-based paleoseismology. Sci. Rep. 10, 2124 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    McSaveney, E. Historic earthquakes: the 1942 Wairarapa earthquakes. Te Ara Encyclopedia of New Zealand https://teara.govt.nz/en/historic-earthquakes/page-9 (2006).New Zealand’s environmental reporting series: our atmosphere and climate. (Ministry for the Environment & Stats NZ, 2020).Beng, K. C. & Corlett, R. T. Applications of environmental DNA (eDNA) in ecology and conservation: opportunities, challenges and prospects. Biodivers. Conserv. 29, 2089–2121 (2020).Article 

    Google Scholar 
    Freeland, J. R. The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. Genome https://doi.org/10.1139/gen-2016-0100 (2016).Article 
    PubMed 

    Google Scholar 
    Barnes, M. A. et al. Environmental conditions influence eDNA persistence in aquatic systems. Environ. Sci. Technol. 48, 1819–1827 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Barnes, M. A. et al. Environmental conditions influence eDNA particle size distribution in aquatic systems. Environmental DNA https://doi.org/10.1002/edn3.160 (2020).Article 

    Google Scholar 
    Corinaldesi, C., Beolchini, F. & Dell’anno, A. Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences. Mol. Ecol. 17, 3939–3951 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Eichmiller, J. J., Best, S. E. & Sorensen, P. W. Effects of temperature and trophic state on degradation of environmental DNA in lake water. Environ. Sci. Technol. 50, 1859–1867 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Strickler, K. M., Fremier, A. K. & Goldberg, C. S. Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. Biol. Conserv. 183, 85–92 (2015).Article 

    Google Scholar 
    Seymour, M. et al. Acidity promotes degradation of multi-species environmental DNA in lotic mesocosms. Commun. Biol. https://doi.org/10.1038/s42003-017-0005-3 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dommain, R. et al. The challenges of reconstructing tropical biodiversity with sedimentary ancient DNA: a 2200-year-long metagenomic record from Bwindi Impenetrable Forest, Uganda. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2020.00218 (2020).Article 

    Google Scholar 
    Jöhnk, K. D. et al. Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14, 495–512 (2008).ADS 
    Article 

    Google Scholar 
    Sogin, M. L. et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”. PNAS 103, 12115–12120 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Deep-sea infauna with calcified exoskeletons imaged in situ using a new 3D acoustic coring system (A-core-2000)

    Joos, F., Plattner, G. K., Stocker, T. F., Marchal, O. & Schmittner, A. Global warming and marine carbon cycle feedbacks on future atmospheric CO2. Science 284(5413), 464–467 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    Smith, K. L. et al. Climate, carbon cycling, and deep-ocean ecosystems. Proc. Nat. Acad. Sci USA 106, 19211–19218 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    Ramirez-Llodra, E. et al. Man and the last great wilderness: Human impact on the deep sea. PLoS ONE 6, e22588 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    Pham, C. K. et al. Marine litter distribution and density in European Seas, from the shelves to deep basins. PLoS ONE 9, e95839 (2014).ADS 
    Article 

    Google Scholar 
    Angel, M. What is the deep sea? In Deep-sea fishes (eds Randall, D. & Farrell, A.) 1–41 (Academic Publishing, 1997).
    Google Scholar 
    Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K. & Arbizu, P. M. Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23, 518–528 (2008).Article 

    Google Scholar 
    Thurber, A. R. et al. Ecosystem function and services provided by the deep sea. Biogeosciences 11, 3941–3963 (2014).ADS 
    Article 

    Google Scholar 
    Solan, M. et al. Extinction and ecosystem function in the marine benthos. Science 306(5699), 1177–1180 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    Danise, S., Twitchett, R. J., Little, C. T. & Clemence, M. E. The impact of global warming and anoxia on marine benthic community dynamics: An example from the Toarcian (Early Jurassic). PLoS ONE 8(2), e56255 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    Nomaki, H. et al. In situ experimental evidences for responses of abyssal benthic biota to shifts in phytodetritus compositions linked to global climate change. Glob. Chang. Biol. 27, 6139–6155 (2021).Article 

    Google Scholar 
    Viehman, H. A. & Zydlewski, G. B. Fish interactions with a commercial-scale tidal energy device in the natural environment. Estuaries Coast 38(1), 241–252 (2015).Article 

    Google Scholar 
    Danovaro, R. et al. Implementing and innovating marine monitoring approaches for assessing marine environmental status. Front. Mar. Sci. 3, 213 (2016).Article 

    Google Scholar 
    Mizuno, K. et al. An efficient coral survey method based on a large-scale 3-D structure model obtained by Speedy Sea Scanner and U-Net segmentation. Sci. Rep. 10(1), 12416. https://doi.org/10.1038/s41598-020-69400-5 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Eleftheriou, A., & Moore, D. C. (2013). Macrofauna techniques. Methods for the study of marine benthos, 175–251.Solan, M. et al. In situ quantification of bioturbation using time lapse fluorescent sediment profile imaging (f SPI), luminophore tracers and model simulation. Mar. Ecol. Prog. Ser. 271, 1–12 (2004).ADS 
    Article 

    Google Scholar 
    Hale, R. et al. High-resolution computed tomography reconstructions of invertebrate burrow systems. Sci. Data 2(1), 1–5 (2015).Article 

    Google Scholar 
    Plets, R. M. et al. The use of a high-resolution 3D Chirp sub-bottom profiler for the reconstruction of the shallow water archaeological site of the Grace Dieu (1439), River Hamble, UK. J. Archaeol. Sci. 36(2), 408–418 (2009).Article 

    Google Scholar 
    Mizuno, K. et al. Automatic non-destructive three-dimensional acoustic coring system for in situ detection of aquatic plant root under the water bottom. Case Stud. Nondestruct. Test. Evaluat. 5, 1–8 (2016).CAS 
    Article 

    Google Scholar 
    Suganuma, H., Mizuno, K. & Asada, A. Application of wavelet shrinkage to acoustic imaging of buried asari clams using high-frequency ultrasound. J. Appl. Phys. 57(7S1), 07LG08 (2018).Article 

    Google Scholar 
    Dorgan, K. M. et al. Impacts of simulated infaunal activities on acoustic wave propagation in marine sediments. J. Acoust. Soc. Am. 147(2), 812–823 (2020).ADS 
    Article 

    Google Scholar 
    Mizuno, K., Cristini, P., Komatitsch, D. & Capdeville, Y. Numerical and experimental study of wave propagation in water-saturated granular media using effective method theories and a full-wave numerical simulation. IEEE J. Ocean. Eng. 45(3), 772–785 (2020).ADS 
    Article 

    Google Scholar 
    Schulze, I. et al. Laboratory measurements to image endobenthos and bioturbation with a high-frequency 3D seismic lander. Geosciences 11(12), 508 (2021).ADS 
    Article 

    Google Scholar 
    Hashimoto, J. et al. Deep-sea communities dominated by the giant clam, Calyptogena soyoae, along the slope foot of Hatsushima Island, Sagami Bay, central Japan. Palaeogeogr. Palaeoclimatol. Palaeoecol. 71(12), 179–192 (1989).Article 

    Google Scholar 
    Fujikura, K., Hashimoto, J. & Okutani, T. Estimated population densities of megafauna in two chemosynthesisbased communities: A cold seep in Sagami Bay and a hydrothermal vent in the Okinawa Trough. Benthos. Res. 57(1), 21–30 (2002).Article 

    Google Scholar 
    Childress, J. J. & Girguis, P. R. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214(2), 312–325 (2011).CAS 
    Article 

    Google Scholar 
    Okuba, K. (2021). Basic study on sonar system development for exploring infaunal bivalves. Master thesis, GSFS, The University of Tokyo (in Japanese).Stoll, R. D. & Bryan, G. M. Wave attenuation in saturated sediments. The J. Acoust. Soc. Am. 47(5B), 1440–1447 (1970).ADS 
    Article 

    Google Scholar 
    Schwartz, L. & Plona, T. J. Ultrasonic propagation in close-packed disordered suspensions. J. Appl. Phys. 55(11), 3971–3977 (1984).ADS 
    Article 

    Google Scholar 
    Seike, K., Shirai, K. & Murakami-Sugihara, N. Using tsunami deposits to determine the maximum depth of benthic burrowing. PLoS ONE 12(8), e0182753. https://doi.org/10.1371/journal.pone.0182753 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Freshwater unionid mussels threatened by predation of Round Goby (Neogobius melanostomus)

    Our research involved work with animal subjects (unionid mussels and Round Goby fishes) and was conducted following relevant regulations and standard procedures. The field collections were carried out under Pennsylvania Fish and Boat Commission permits (# 2018-01-0136 and 2019-01-0026). The experimental protocols were approved by Penn State University’s Institutional Animal Care and Use Committee (IACUC# 201646941 and 201646962). All new DNA sequencing data are made publicly available in GenBank (with accession numbers provided in Table 1) and a BioProject (# PRJNA813547) of the National Center for Biotechnology Information40.Propensity of Round Goby to consume unionid mussels in a controlled lab settingStream table setupWe conducted lab experiments to observe the potential predation of juvenile freshwater mussels by the Round Goby, following standard research protocols for work with animal subjects (IACUC# 201646962, Penn State University). We constructed four artificial stream tables in an aquatic laboratory, each measuring 3 × 2 m and featuring two run and two pool sections (each 0.63 × 0.56 × 0.46 m). Water flow was produced using eight Homsay 920 GPH submersible water pumps, which pumped water from a central reservoir tub into each table at the start of each run section. The water flow direction was clockwise for stream tables 1 and 3, and counterclockwise for stream tables 2 and 4. Water pumped into the stream tables exited via two drains located medially of each run section, where it flowed back to the central reservoir tub. Each stream table was filled with a 6 mm layer of substrate consisting of a mixture of sand, gravel (4–6 mm), and crushed stone (size 2B, with an average size of ~ 19 mm). The day before each experiment, field technicians traveled to local streams and collected macroinvertebrates using one minute D-frame kick net samples for each of the four stream tables. The macroinvertebrates and associated substrate were transported back to the facility and were introduced into each stream table system.Preferential feeding experimentsBefore each experiment commenced, juvenile Plain Pocketbook mussels (Lampsillis cardium) were introduced into each stream table (with 165 mussel specimens for experiment 1 and 100 mussels for experiments 2 and 3). This  widespread and abundant species is not imperiled in Pennsylvania, and mussels were provided for this study by the White Sulphur Springs National Fish Hatchery located in southeast West Virgina. The mussels were allowed to acclimate in the stream tables for 2 h before commencing each experiment. Ten Round Gobies were introduced into each stream system (stream tables 1 and 2 for experiment 1, and all tables for experiments 2 and 3). The total length (from nose tip to caudal tip) of each fish was measured prior to introduction and after the termination of experiments 2 and 3. Experiment 1 was conducted for 3 weeks, while experiments 2 and 3 were conducted for 8 days. During these experiments, Round Gobies were allowed to exist in the systems and feed preferentially, on the mussels and macroinvertebrates, for the allotted time before each investigation concluded. We acknowledge that in these experiments, the mussel abundances are higher and macroinvertebrate densities lower and less rich than commonly occur in the natural stream environment. Further, the Round Goby fish densities used are much higher than currently in the French Creek watershed, though are comparable to what is currently seen in parts of the Great Lakes basin. Nonetheless, the experiment scenarios allowed us to observe if Round Gobies would consume the mussels when given the choice to feed on a variety of food items.Evaluation of unionids consumed by fishRound Gobies were removed from the stream tables upon completion of each experiment. They were euthanized using  > 250 mg/L buffered (pH ~ 7) tricaine-S (MS222) solution. The fish were submerged for 10 min beyond the cessation of opercular movement to ensure proper euthanasia, and tissues were collected after we confirmed complete euthanasia—compliant with AVMA guidelines and approved by the IACUC protocol. The Round Gobies were placed in a 10% solution of formalin for preservation, and after 2 weeks, they were rinsed with clean water and were placed in 70% ethanol for long-term storage. After fish were removed from the system, the water was drained, and the substrate was sifted to recover the remaining mussels. Mussels were counted, and live individuals were returned to holding tanks for use in subsequent experiments. To further assess whether Round Gobies had consumed mussels during the investigation, Round Gobies were x-rayed using a Bruker Skyscan 1176 micro-CT scanner. After that, the stomachs of each fish were excised, and the contents examined using a Leica CME dissection scope to confirm the identity of Plain Pocketbook mussels. Contents posterior to the stomach were not analyzed because they could not be reliably counted and identified.DNA metabarcoding to identify mussel species consumed by Round Goby in a stream settingFish and mussel sample acquisitionWe collected 39 Round Gobies directly from streams within the French Creek watershed—their newly invaded natural stream habitats—in June 2018. We aimed to quantify which species, if any, of unionid mussels they consumed. Fish collection locations included LeBoeuf Creek at Moore Road and 100 m below the confluence of French Creek and LeBoeuf Creek. The unionid mussel populations and the environmental field settings at these locations are detailed by Clark et al.19. A team of field technicians collected fish by kick seining (3 m × 1 m × 9.5 mm nylon mesh) while moving downstream. Seining was the sampling method of choice compared to electrofishing to avoid possible regurgitation of food items prior to excision of fishes’ stomachs. The stream reaches sampled at each location were between 100 and 200 m in length and included riffle, run, and pool habitats. In addition to fish samples, unionid mussel samples from French Creek were also collected for analysis (under Pennsylvania Fish & Boat Commission collectors permits # 2018-01-0136 and 2019-01-0026). Following standard research protocols (under IACUC# 201646941, Penn State University), the Round Gobies collected were euthanized using buffered Tricaine-S (MS222) solution; and stomachs were excised using sterilized utensils before being placed in sterilized tubes filled with 97% ethanol. After excision of stomachs, fishes were placed in a 10% formalin solution for preservation. After 2 weeks, fishes were rinsed with clean water and transferred to 70% ethanol for storage. The stomach samples were immediately placed in ethanol and on ice in the field. Samples were stored in a freezer before being shipped to the US Geological Survey’s Eastern Ecological Science Center for various molecular ecology analyses. Once the fish and mussel samples arrived at this lab, they were recorded and stored at four °C until analysis.Primer developmentSpecific primers targeting a moderately conserved region of the mitochondrial COI gene for 25 species of unionids inhabiting French Creek were designed. Previously a PCR-based amplification method utilizing restriction enzyme digests was used to identify genetic fingerprints of 25 unionid species inhabiting French Creek41. Here, we designed a new degenerate PCR primer set modified with sequencing overhangs to facilitate compatibility with a MiSeq amplicon sequencing method previously designed for 16S Amplicon sequencing. We targeted the locus of the mitochondrial COI gene of unionids known to inhabit the Atlantic Slope Drainage. Consensus sequences were derived using Multalin analysis and a tiling method to identify conserved primer binding regions flanking an ~ 300 bp region of the COI gene. This gene was targeted in part due to the availability of partial or complete sequences representing these target species in the NCBI reference database40. Cytochrome oxidase sequences were downloaded for the 25 unionid mussel species of interest. However, a COI sequence for the Rabbitsfoot (Theliderma cylindrica) mussel was absent from the NCBI database, which required us to sequence this region for an in-house reference (which is described later in the paper). We designed a degenerate primer cocktail specific to all mussel species of interest that amplified a ~ 289 bp product, with forward and reverse primers used for the amplification of unionid specific COI presented as supplemental information (see Table S-230. We evaluated the suitability of the primers using samples from field identified mussels. For primer optimization, PCR was run across a gradient of annealing temperatures to determine suitability. In addition, we used Round Goby DNA as a template to evaluate specificity. In addition to Round Goby stomach samples, mussel samples of several species collected from French Creek were included as positive controls.DNA extraction from tissue samplesFollowing the manufacturer’s protocols, tissue samples (including fish stomach and mussel tissue) were extracted with the Zymo Research ZymoBIOMICS 96 MagBead DNA Kit (San Diego, CA). Random samples of DNA extracts were analyzed on an Agilent 2100 Bioanalyzer using a high-sensitivity assay kit. Fragments in the target amplicon range were apparent (albeit not known to be of mussel origin). All samples were stored at − 20 °C until PCR was performed. DNA from both the T. cylindrica and L. complanata samples were analyzed for DNA quality.Rolling circle amplification of mitochondrial genomesTo acquire COI sequences for T. cylindrica and L. complanata, we subjected archived DNA samples to rolling circle amplification (RCA) followed by amplicon sequencing on the MiSeq. In short, 2 µl of DNA template was added to 2 µl Equiphi29 DNA polymerase reaction buffer containing 1 µl of Exonuclease-resistant random primers (ThermoFisher). Samples were denatured by heating to 95 °C for 3 min followed immediately by cooling on ice for more than 5 min. A volume of 5 µl was added to an RCA master mix containing 1.5 µl of 10 × Equiphi29 DNA polymerase reaction buffer, 0.2 µl of 100 mM dithiothreitol, 8 µl of 2.5 mM dNTPs, 1 µl of Eqiphi29 DNA polymerase (10U) and 4.3 µl of nuclease-free water. The samples were heated to 45 °C for 3 h and then 65 °C for 10 min. Samples were then placed in ice and then frozen at − 20 °C. All RCA products were normalized to 0.2 ng/µl in 10 mM Tris–HCl, pH 8.5. Normalized RCA product was utilized as a template for an Illumina Nextera XT library preparation. Sequencing libraries were prepared following the Nextera XT Library Preparation Reference Guide (CT# 15031942 v01) using the Nextera XT Library Preparation Kit (Illumina, San Diego, CA). Final libraries were analyzed for size and quality using the Agilent BioAnalyzer with the accompanying DNA 1000 Kit (Agilent, Santa Clara, CA). Libraries were quantified using the Qubit H.S. Assay Kit (Invitrogen, Carlsbad, CA) and normalized to 4 nM using 10 mM Tris, pH 8.5. Libraries were pooled and run on the Illumina MiSeq at a concentration of 10 pM with a 5% PhiX spike with run parameters of 1 × 150. Bioinformatic processing of this data is outlined below.Amplification of the cytochrome oxidase 1 geneExtracted genomic DNA was used as template for end-point PCR. Samples evaluated were from mussels and round gobies (see supporting Table S-330). The ~ 289 bp COI region was amplified with the mussel primers as follows. The amplification reaction contained 0.15 µM of each primer, 1 µL of the initial amplification product, and Promega Go Taq Green Master Mix following manufacturer recommendations for a 25 µL reaction. The thermocycler program consisted of an initial denaturing step of 95 °C for 3 min, followed by 30 cycles of 30 s at 95 °C, 30 s at 52 °C, and 1 min at 72 °C. Products were subjected to a final extension of 72 °C for 5 min then held until collection at 12 °C. An appropriately sized amplification product was confirmed for each reaction by electrophoresis of 5 µL of the reaction product through a 1.5% I.D. N.A. agarose gel (FMC Bioproducts) at 100 V for 45 min. PCR products were cleaned with the Qiagen Qiaquick PCR purification kit (Valencia, CA) and quantified using the Qubit dsDNA H.S. Assay Kit (Thermofisher Scientific, Grand Island, NY). Samples were diluted in 10 mM Tris buffer (pH 8.5) to a final concentration of 5 ng/µL.Generation of mock mussel samplesTo better understand and minimize sources of error or bias in the taxonomic assignment, we created a mock extraction by mixing sequences from known mussel taxa at defined concentrations. For each mussel, approximately 25-mg of tissue was extracted with the ZymoBIOMICS 96 MagBead DNA Kit (San Diego, CA) following the manufacturer’s protocol. The COI sequence was amplified from each species using the same primer-protocol combination described above. A total of 5 PCR products were mixed at equal concentration (mass/volume) to generate the mock sample (“Mock” hereafter). To confirm the identity of these inputs, each COI region was amplified and sequenced on the Illumina MiSeq during the same run as the Mock and samples.Sequencing library preparation and quality assessmentNext-generation sequencing was performed on the Illumina MiSeq platform to observe species-specific sequences and determine the diet of the Round Goby. Inclusion of the overhangs on the amplification primers allowed us to utilize the Illumina 16S Metagenomic Sequencing Library Preparation protocol42. Amplicon libraries were prepared following the same manufacturer’s protocol. All samples were indexed using the Illumina Nextera XT multiplex library indices. DNA read size spectra were determined with the Agilent 2100 Bioanalyzer using the Agilent DNA 1000 Kit (Santa Clara, Calif.). Libraries were quantified with the Qubit dsDNA H.S. Assay Kit (ThermoFisher Scientific, Grand Island, N.Y.) and normalized to 4 nM (nM) using 10 mM (mM) Tris (hydroxymethyl) aminomethane buffer pH 8.5. A final concentration of 10 picomolar library with a 6.5% PhiX control spike was created with the combined pool of all indexed libraries. All bioinformatic operations were completed on CLC Genomic Workbench v20 (Qiagen, Valencia, Calif.).Read filtering, trimming, and RNAseq metabarcoding assemblyFASTQ files from the sequencing runs were imported as paired-end reads into CLC Genomics Workbench v20.0.4 (Qiagen Bioinformatics, Redwood City, Calif.) for initial filtering of exogenous sequence adaptors and poor-quality base calls. The trimmed overlapping paired-end reads were mapped to the 25 target unionid sequences specific for the species of interest. Several mapping iterations were run using different levels of stringency. We utilized + 2/− 3 match-mismatch scoring and set the length fraction to 0.90. Analyses were iterated using different similarity fractions ranging from 0.90 to 0.99. Reads were annotated, and relative abundance was determined using a curated reference library (see supporting Datasets S-1 and S-230). More

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    Nepotistic colony fission in dense colony aggregations of an Australian paper wasp

    Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Ross, K. G. & Matthews, R. W. The Social Biology of Wasps (Cornell University Press, 1991).Book 

    Google Scholar 
    Itô, Y. & Higashi, S. Spring behaviour of Ropalidia plebeiana (Hymenoptera: Vespidae) within a huge aggregation of nests. Appl. Entomol. Zool. 22, 519–527 (1987).Article 

    Google Scholar 
    Saito, F. & Kojima, J.-I. Colony cycle in the south-eastern coastal populations of Ropalidia plebeiana, the only Ropalidia wasp occurring in temperate Australia. Entomol. Sci. 8, 263–275 (2005).Article 

    Google Scholar 
    Richards, O. W. The Australian social wasps (Hymenoptera: Vespidae). Aust. J. Zool. Suppl. Ser. 26, 1–132 (1978).Article 

    Google Scholar 
    Makino, S., Yamane, S., Itô, Y. & Spradbery, J. P. Process of comb division of reused nests in the Australian paper wasp Ropalidia plebeinana (Hymenoptera, Vespidae). Ins. Soc. 41, 411–422 (1994).Article 

    Google Scholar 
    Goodnight, K. F. & Queller, D. C. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol. 8, 1231–1234 (1999).Article 

    Google Scholar 
    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Crochet, P.-A. Genetic structure of avian populations—Allozymes revisited. Mol. Ecol. 9, 1463–1469 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Meirmans, P. G. & Hedrick, P. W. Assessing population structure: FST and related measures. Mol. Ecol. Res. 11, 5–18 (2011).Article 

    Google Scholar 
    Hedrick, P. W. A standardized genetic differentiation measure. Evolution 59, 1633–1638 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Itô, Y., Yamane, S. & Spradbery, J. P. Population consequences of huge nesting aggregations of Ropalidia plebeiana (Hymenoptera: Vespidae). Res. Popul. Ecol. 30, 279–295 (1988).Article 

    Google Scholar 
    Boomsma, J. J. & d’Ettorre, P. Nice to kin and nasty to non-kin: revisiting Hamilton’s early insights on eusociality. Biol. Lett. 9, 20130444 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hannonen, M. & Sundström, L. Worker nepotism among polygynous ants. Nature 421, 910 (2003).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Parsons, P. J., Grinsted, L. & Field, J. Partner choice correlates with fine scale kin structuring in the paper wasp Polistes dominula. PLoS ONE 14, e0221701 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Strassmann, J. E., Queller, D. C., Solis, C. R. & Hughes, C. R. Relatedness and queen number in the Neotropical wasp, Parachartergus colobopterus. Anim. Behav. 42, 461–470 (1991).Article 

    Google Scholar 
    Leadbeater, E., Carruthers, J. M., Green, J. P., Rosser, N. S. & Field, J. Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science 333, 874–876 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Field, J. & Leadbeater, E. Cooperation between non-relatives in a primitively eusocial paper wasp, Polistes dominula. Philos. Trans. R. Soc. B 371, 20150093 (2016).Article 

    Google Scholar 
    Bhadra, A. & Gadagkar, R. We know that the wasps “know”: cryptic successors to the queen in Ropalidia marginata. Biol. Lett. 4, 634–637 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bang, A. & Gadagkar, R. Reproductive queue without overt conflict in the primitively eusocial wasp Ropalidia marginata. Proc. Nat. Acad. Sci. USA 109, 14494–14499 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Frank, S. A. Hierarchical selection theory and sex ratios. II. On applying the theory, and a test with fig wasps. Evolution 39, 949–964 (1985).PubMed 
    Article 

    Google Scholar 
    Silk, J. B. & Brown, G. R. Local resource competition and local resource enhancement shape primate birth sex ratios. Proc. R. Soc. Lond. B. 275, 1761–1765 (2008).
    Google Scholar 
    Schwarz, M. P. Local resource enhancement and sex ratios in a primitively social bee. Nature 331, 346–348 (1988).ADS 
    Article 

    Google Scholar 
    Cronin, A. L. & Schwarz, M. P. Sex ratios, local fitness enhancement and eusociality in the allodapine bee Exoneura richardsoni. Evol. Ecol. 11, 567–577 (1997).Article 

    Google Scholar 
    Schwarz, M. P., Bull, N. J. & Hogendoorn, K. Evolution of sociality in the allodapine bees: A review of sex allocation, ecology and evolution. Ins. Soc. 45, 349–368 (1998).Article 

    Google Scholar 
    Gamboa, G. J., Wacker, T. L., Duffy, K. G., Dobson, S. W. & Fishwild, T. G. Defence against intraspecific usurpation by paper wasp cofoundresses (Polistes fuscatus, Hymenoptera: Vespidae). Can J. Zool. 70, 2369–2372 (1992).Article 

    Google Scholar 
    Katada, S. & Iwahashi, O. Characteristics of usurped colonies in the subtropical paper wasp, Ropalidia fasciata (Hymenoptera: Vespidae). Ins. Soc. 43, 247–253 (1996).Article 

    Google Scholar 
    Yamane, S. Ecological factors influencing the colony cycle of Polistes wasps. in Natural History and Evolution of Paper-Wasps (Turillazzi, S. & West-Eberhard, M. J. eds.). 75–97. (Oxford University Press, 1996).Clouse, R. Some effects of group size on the output of beginning nests of Mischocyttarus mexicanus (Hymenoptera: Vespidae). Flor. Entomol. 84, 418–425 (2001).Article 

    Google Scholar 
    Strassmann, J. E. Female-biased sex ratios in social insects lacking morphological castes. Evolution 38, 256–266 (1984).PubMed 

    Google Scholar 
    Suzuki, T. Production schedule of males and reproductive females, investment sex ratios, and worker-queen conflict in paper wasps. Am. Nat. 128, 366–378 (1986).Article 

    Google Scholar 
    Tsuchida, K. & Suzuki, T. Conflict over sex ratio and male production in paper wasps. Ann. Zool. Fenn. 43, 468–480 (2006).
    Google Scholar 
    Ohtsuki, H. & Tsuji, K. Adaptive reproduction schedule as a cause of worker policing in social Hymenoptera: A dynamic game analysis. Am. Nat. 173, 747–758 (2009).PubMed 
    Article 

    Google Scholar 
    Walsh, P. S., Metzger, D. A. & Higuchi, R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513 (1991).CAS 
    PubMed 

    Google Scholar 
    Bassam, B. J., Caetano-Anolles, G. & Gresshoff, P. M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal. Biochem. 196, 80–83 (1991).CAS 
    PubMed 
    Article 

    Google Scholar 
    van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M. & Shipley, P. MICRO-CHECHER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes. 4, 535–538 (2004).Article 
    CAS 

    Google Scholar 
    Peakall, R. & Smouse, P. E. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes. 6, 288–295 (2006).Article 

    Google Scholar 
    Raymond, M. & Rousset, F. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered. 86, 248–249 (1995).Article 

    Google Scholar 
    Meirmans, P. G. GenoDive version 3.0: Easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol. Ecol. Res. 20, 1126–1131 (2020).CAS 
    Article 

    Google Scholar 
    Michalakis, Y. & Excoffier, L. A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142, 1061–1064 (1996).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Earl, D. & vonHoldt, B. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Res. 4, 359–361 (2012).Article 

    Google Scholar 
    Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A. & Mayrose, I. Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Res. 15, 1179–1191 (2015).CAS 
    Article 

    Google Scholar 
    Goodnight, K. F. Relatedness 4.2c Release (Rice University, 1996).
    Google Scholar 
    Queller, D. C. A method for detecting kin discrimination within natural colonies of social insects. Anim. Behav. 47, 569–576 (1994).Article 

    Google Scholar  More

  • in

    Understanding the spatial distribution and hot spots of collared Bornean elephants in a multi-use landscape

    By pooling the results of the entire known range analysis of 14 GPS-collared elephants living in the Kinabatangan, our study suggests that this populations range covers at least 628 km2 (Table 3). Nine different locations were identified as hot spots, representing 266.9 km2 or 43% of this range, suggesting that just under half is highly used and/or frequented (Fig. 1). We found that the size of individual’s hot spots was positively related to the size of the entire range, meaning the larger the entire range the larger the summed area of an elephants hot spots. On average, hot spots represented a relatively small percent of an animal’s entire range (ranging from 4 to 20%, averaging 12%, Table 3). However, time spent within these hot spots ranged from 10 to 60% (averaging 34% across elephants, Table 5), with time spent in hot spots being related to the overall size of the hot spots (the larger the hot spot the more time elephants spent in them).Identifying the location of these hot spots is essential in designing appropriate management practices in collaboration with land users and identifying the best location for elephant corridors. In the last 25 years, forest cover in the Lower Kinabatangan has been drastically reduced and fragmented46, eroding the biodiversity value of this landscape. Today, this region has little remaining forests, and what is left is insufficient for sustaining the local elephant population10. Moreover, forests are highly fragmented along the Kinabatangan River, with a number of bottlenecks constraining elephant movements9. The situation in this landscape is getting worse because of further land clearances for agriculture, namely oil palm; as well as for the highly controversial Sukau Bridge and new road/highway that is planned for the region.Our analyses revealed a highly significant difference between the average proportions of protected area, unprotected forest, and oil palm estate extents within the elephant’s entire range; and a substantive, but not significant, difference across these land use/land cover types within hot spots (Table SI 4). At the individual level, there was a highly significant negative relationship between the proportion of protected areas and oil palm estates both within the elephant’s entire range and within the hot spots.At the pooled level, we found that around 45% of the entire known range and hot spots were within forested environments (280.44 km2 and 120.29 km2 respectively). Our results showed strong fidelity of certain elephants to these forested habitats. Our k-means cluster analysis found that within elephant entire ranges and hot spots, two out of the three cluster groups had high or very high usage of forests. Both cluster 1, for the entire range, and cluster 1 for hot spots extents, had five females that on average used forest environments 90% of their time, with protected areas being used 64% and 59%, and unprotected forested being used on average 26% and 31%, respectively (Table 7).Individuals in cluster 2, for the entire range analysis, on average, spent 73% of their time in forests (57% of this in protected areas and 16% in unprotected forests; Table 7). For the hot spot analysis, the individuals in cluster 2 spent on average 65% of their time in forests (52% of this in the unprotected forests and 13% in protected forests; Table 7). Elephants within these clusters were all females. Our results suggest that forest may be of particular importance for females as they had forest as their dominant land cover type within their entire range, hot spot extents and time spent analyses (Fig. 3, Table 5). Several studies have shown that adult females influence and guide the movement patterns and habitat utilization for their family group and that females in family units tend to inhabit less risky areas, such as within natural forest habitat60,61,62.However, the unprotected forest is at risk. We identified about 8% (or 49 km2) of forest identified within the pooled entire known range were not protected, with half potentially being on state land, and the remaining half on land titles of various types (Table SI 4). For the pooled hot spot areas, unprotected forest was proportionally higher, comprising of 11% (or 29 km2) of the total extent, with 54% being potentially on State land and 46% on land titles (Table SI 4). Protecting these forests would be an essential and efficient way to secure key elephant habitat since all collared individuals were using these forest fragments in their entire range (averaging 11%, and ranging from 8 to 18%), and hot spot extents (averaging 20%, and ranging from 0 to 53%) (Table SI 4, Fig. 3). On average, 24% of time was spent in unprotected forests within hot spots, though this varied widely from 0% (for the male elephant known as Gading) to 61% (for the female matriarch named Jasmine) (Table 5). In fact, five females had large proportions of their hot spot extents (24–53%) in unprotected forests, spending substantial periods of their time (33–61%) within these threatened areas.Our findings show that unprotected forests around the villages of Bilit and Sukau, were of particular significance (Figs. 1, 2). These unprotected forests largely consist of lowland dry forest, seasonally flooded swamp forest, and swamp forest, which are considered important habitats for elephants for feeding, resting and moving47,63. Within these forests, and along the forest margins and river banks there are also natural open grasslands that consist of Phragmites karka and Dinochloa scabrida that provide essential forage, mainly in the riparian areas for elephants9,21,23. Forested environments are also considered to be important in providing natural refugee from human activities and disturbance. For example, elephants have been documented to form significantly larger group sizes, as well as engaging in significantly more social interactions, in natural forest habitat compared to, for example, oil palm landscapes63. Adult females, generally, avoid areas considered unsafe for their respective social units, are more selective in the resources they use, and require regular access to water because of the presence of young64,65,66. This may be why our results, strongly suggest that forest habitats seem to be most important for adult females.Another significant issue faced by these elephants is the threat from the controversial planned Sukau bridge and road/highway that is set out in the Sabah Structure Plan, an overarching policy document for the State58. Currently, a new road/highway is under construction on the northern bank of the village of Sukau, and this has already cleared areas of unprotected forest. This public road could link to a potential new bridge that would cross over the Kinabatangan River, cutting through unprotected forest and a protected area (Lower Kinabatangan Wildlife Sanctuary), before going through oil palm estates then through another protected area to the south and through the Tabin elephant population range. For the Kinabatangan, creating a public highway will cut the elephant population range into two parts (Figs. 2, 3). All collared elephants use this area, as it is a key bottleneck and the only alternative option to pass around Sukau village9. We found that nine elephants have hot spots that intersect or meet up with the current road (which will be up-graded and get considerably busier) and/or the planned road/highway alignment (Figs. SI 1 and 2). For these elephants, we calculated that they spent from 2 to 44% (average 14%) of their time within these hot spots (Table 4). Our statistical analyses suggest that if the road/highway goes ahead it will have a significant impact on the elephants’ behaviour with respect to time spent in the hot spots. Indeed, this infrastructure project could have dire consequences for these elephants and their family groups, by disrupting their ranging patterns and segmenting the entire elephant range into two (Figs. 2, 4). The existing road in Batu Putih has already proven to be an impassable barrier for this elephant population, as no elephants have been observed crossing this road since the early 2000s14. For elephants that do try and cross, vehicle collisions may become a significant threat to elephants and drivers alike67, and potentially increasing human–elephant conflict in the nearby villages, as well as in plantations14,68,69, exacerbating an already difficult situation for this small and fragmented population.Results from the pooled analysis show that about 53% of the entire known population range is within oil palm estates; and 51% for the pooled hot spots (Fig. 3, Table SI 4). Our k-means clustering analysis grouped 6 elephants into cluster 3 that on average spent 57% of time in oil palm estates; and 7 elephants into cluster 2 within the hot spot analysis that on average spent 73% of their time in oil palm estates (Table 6). All the males, were clustered within these groups (Table 5). In fact, the three collared males were amongst the highest users of oil palm estates (Fig. 3, Table SI4, and 5). This could be related to a ‘‘high risk, high gain’’ strategy, often adopted by males to increase body size and enhance reproductive success32,33,60. However, it is interesting to see that three females (Ita, Ratu and Koyah) and their respective social units, also seemed to have high levels of oil palm use, while other individuals had zero or very little use of oil palm (e.g. Aqeela, Jasmin, Sandi, Kasih; Table SI 4, Fig. 3). Differential choices may result from differences in individual knowledge and experience with people during past encounters, for example70,71.We identified that collared elephants were ranging in 11 known oil palm estates, with the five most regularly used being Melangking Oil Palm Plantation (with 12 elephants entire range overlapping with this estate and six hot spots), IOI Corporation (with 11 overlapping entire ranges, and eight hot spots), Genting Plantations (14 and seven, respectively), Sime Darby Plantation (five and two, respectively), and Karangan Agriculture (8 and 2, respectively) (Table 6; Fig. 4). Presence of bottlenecks and barriers (e.g. electric fences) may explain hot spot occurrences in these estates, as well as feeding opportunities, management strategies of specific estates, and historical and seasonal ranges.Linear features like major highways, electric fences and drainage ditches hamper elephant movements within the Lower Kinabatangan9. A previous study identified 20 bottlenecks in the Lower Kinabatangan with the two main ones (of 9 km and 6.5 km in length) found around the village of Sukau9. In addition, the unplanned and chaotic erection of electric fences by large estates and smallholdings has disrupted significantly elephant movement patterns and resulted in artificial hot spots for certain individuals (e.g. Liun, Ita, Gading and Sejati)35,72. Electric fences have widely been used to mitigate human–elephant conflicts. The establishment of fences rarely consider the traditional elephant routes nor the location of existing fences in neighbouring estates. If elephants manage to enter such areas, they often become trapped and experience difficulties in returning to nearby forests, exacerbating conflicts with people35.Certain estates such as Melangking Oil Palm Plantation have allowed elephants to roam freely in their estate (Muhammad Al-Shafieq, personal communication). Since 2017, this plantation has shown a drastic reduction in damages to their oil palms following the removal of their permanent electric fences surrounding their entire estate. Instead, this plantation is using a temporary electric fencing regime around newly planted palm areas. Concurrently, they now do not push elephants out of their estate, which can explain why Melangking Oil Palm Plantation is a significant hotspot in the region.Another reason why elephant ranges incorporate oil palm estates is to move between forest patches that are becoming completely isolated following forest conversion, as is the case close to Sukau (Fig. SI1 and SI2; Fig. 1). Unlike other elephant species that increase their speed of movement rates in highly disturbed areas27,30,66, the Bornean elephant has been observed doing the opposite, which may explain some of the hot spots within oil palm estates. This movement strategy may allow for better vigilance as seen on a few occasions when elephants spent 2–5 days in the Bukit Melapi-Yu Kwang Corridor, near the village of Sukau, before leaving the area (Othman, personal observation).Hot spots in the oil palm landscape can also be explained by feeding opportunities, since elephants feed on palm shoots, leaves and hearts73. Elephants are known to eat the shoots of newly planted oil palms, often killing the palms and causing significant economic damages35. Since 2010, many estates located in the Lower Kinabatangan have started a new palm rotation. Palms are replanted every 25 years. A new rotation includes land clearing, bole and root mass removal, and the shredding or chipping of felled palms. Elephants are attracted to the shredded palm hearts since it gives them easy access to one of their favourite food72. This particular behaviour does not cause economic damage, and some estate managers allow the elephants to stay and forage in the chipping areas. This was documented for several collared elephants, whose hot spots and time spent were particularly high within oil palm (e.g. Gading and Sandy, two males; and Ratu and Ita, two females). Once the shredded palms have dried, however, elephants will leave these areas and move elsewhere. Within oil palm estates, some elephants have been found to travel more directly and rapidly suggesting ‘exploratory’ behaviour, which could be associated with searching for young palms or areas of palm felling and chipping of palm hearts15.Lastly, elephants may still be using their historical range that used to be covered with forest before conversion to oil palm. Other factors potentially explaining the relatively high use of oil palm estates include seasonal variations of ranging patterns. Indeed events of drought or floods limit the access to various parts of the floodplain and will tend to confine the animals in some areas9,63.In Sabah the state authorities have recorded at least 200 elephant deaths from the year 2010 to 2021 and most of these have occurred on, or near, oil palm estates14,74,75,76. Deaths from non-natural causes are largely due to poisoning (both accidental and intentional), gunshot wounds, poaching for tusks and other body parts, and snares35. Stopping killing and enabling a safe coexistence between people and elephants within multiple-use landscapes that are dominated by oil palm is one of the key strategies developed in the Bornean Elephant Action Plan for Sabah (2020–2029), which was endorsed by the State14. Based on our results in Lower Kinabatangan, a series of recommendations are proposed.This study underscores the importance of remaining forested areas for the Lower Kinabatangan elephant population. Full protection of all forest fragments left in the Lower Kinabatangan is urgently needed. Several official mechanisms are available to fulfil this request that has been proposed for the past 20 years by various organizations46.The current network of forests available in the Lower Kinabatangan is too small and fragmented to sustain a viable elephant population. Forest corridors must be created across the landscape through reforestation exercises, whilst concurrently undertaking enrichment planting of native understory forage within forested areas as this may minimize the need for elephants to search for easily accessible food in high-risk oil palm landscapes21,22,23.Current governmental plans to build a road bridge and public road/highway linking the southern bank of the Kinabatangan River to Tabin Wildlife Reserve to the south will irreversibly impact the Lower Kinabatangan elephant population by cutting the current range into two isolated parts. This will impact the elephants ranging patterns, potentially even fragmenting the already small population into two groups, and potentially leading to elephant deaths by vehicle collisions (which is becoming increasingly common in Peninsular Malaysia), and increase the risk of poaching activities, all resulting in a decrease in the genetic diversity of the, already small and isolated, population14,67.Eventually, the future of the Kinabatangan elephant population resides in improving land use and management practices within oil palm estates currently used by elephants. We recommend that priority should be given at improving elephant movements in oil palm estates by removing unnecessary man-made barriers and only cautiously installing temporary electric fences to protect sensitive areas. For example, the use of electric fences around mature oil palm and areas whereby palms are being removed and chipped could be prohibited, and electric fences permitted solely for protecting oil palm nurseries, new plantings and young oil palms (e.g. up to 7–8 years old), and staff and office quarters. This would greatly allow for landscape permeability for elephants, and other species that need to cross the landscape for their ecological and biological needs14.A handful of guidelines exist to assist oil palm managers and staff in managing elephant populations in their respective estates72,77. However, there is a need for a more comprehensive set of guidelines, which delineate better practices with the aim to increase the protection of people and elephants outside protected areas. Guidelines should specify “do’s” and “don’ts” (based on best available data and knowledge) of actions needed before, during and after elephants visit oil palm estates and smallholdings.Sabah now is in an interesting transition within their palm oil sector. On the 21st October 2015, the Sabah State Cabinet committed to produce 100% certified sustainable palm oil, by 2025, under the Roundtable for Sustainable palm Oil (RSPO) Jurisdictional Certification approach. Under this approach, areas of High Conservation Value and areas identified within the High Carbon Stock Approach need specific management and monitoring, in order to comply with RSPO principles and criteria78,79,80. Sabah government can use this platform to build an integrated landscape level approach to better manage landscapes within known elephant ranges (which is considered a High Conservation Value species) to allow for a safe and permeable movement through the landscape.Eventually, long-term survival of the Bornean elephant will mainly depend on how people and elephants can co-exist. It is our hope that this study illustrates the importance of protecting all forested habitat and effectively managing areas outside of protected areas to allow for long-term elephant coexistence with humans in this landscape. More

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    Limited acclimation of early life stages of the coral Seriatopora hystrix from mesophotic depth to shallow reefs

    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Glynn, P. W. Coral reef bleaching: facts, hypotheses and implications. Glob. Chang. Biol. 2, 495–509 (1996).ADS 
    Article 

    Google Scholar 
    Riegl, B. & Piller, W. E. Possible refugia for reefs in times of environmental stress. Int. J. Earth Sci. 92, 520–531 (2003).Article 

    Google Scholar 
    Hinderstein, L. M. et al. Theme section on ‘Mesophotic Coral Ecosystems: Characterization, Ecology, and Management’. Coral Reefs 29, 247–251 (2010).ADS 
    Article 

    Google Scholar 
    Bongaerts, P., Ridgway, T., Sampayo, E. M. & Hoegh-Guldberg, O. Assessing the ‘deep reef refugia’ hypothesis: Focus on Caribbean reefs. Coral Reefs 29, 309–327 (2010).Article 

    Google Scholar 
    Smith, T. B. et al. Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Global Change Biol. 22, 2756–2765 (2016).ADS 
    Article 

    Google Scholar 
    Frade, P. R. et al. Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching. Nat. Commun. 9, 3447 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Holstein, D. M., Paris, C. B., Vaz, A. C. & Smith, T. B. Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35, 23–37 (2016).ADS 
    Article 

    Google Scholar 
    Prasetia, R., Sinniger, F., Hashizume, K. & Harii, S. Reproductive biology of the deep brooding coral Seriatopora hystrix: Implications for shallow reef recovery. PLoS ONE 12, e0177034 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Shlesinger, T., Grinblat, M., Rapuano, H., Amit, T. & Loya, Y. Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt. Ecology 99, 421–437 (2018).PubMed 
    Article 

    Google Scholar 
    Gleason, D. F. & Hofmann, D. K. Coral larvae: From gametes to recruits. J. Exp. Mar. Bio. Ecol. 408, 42–57 (2011).Article 

    Google Scholar 
    Hughes, T. P. & Tanner, J. E. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81, 2250–2263 (2000).Article 

    Google Scholar 
    Bongaerts, P. et al. Deep reefs are not universal refuges: Reseeding potential varies among coral species. Sci. Adv. 3, e1602373 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    van Oppen, M. J. H., Bongaerts, P., Underwood, J. N., Peplow, L. M. & Cooper, T. F. The role of deep reefs in shallow reef recovery: An assessment of vertical connectivity in a brooding coral from west and east Australia. Mol. Ecol. 20, 1647–1660 (2011).PubMed 
    Article 

    Google Scholar 
    Cohen, I. & Dubinsky, Z. Long term photoacclimation responses of the coral Stylophora pistillata to reciprocal deep to shallow transplantation: Photosynthesis and calcification. Front. Mar. Sci. 2, 45 (2015).Article 

    Google Scholar 
    Eyal, G. et al. Euphyllia paradivisa, a successful mesophotic coral in the northern Gulf of Eilat/Aqaba, Red Sea. Coral Reefs 35, 91–102 (2016).ADS 
    Article 

    Google Scholar 
    Ben-Zvi, O. et al. Photophysiology of a mesophotic coral 3 years after transplantation to a shallow environment. Coral Reefs 39, 903–913 (2020).Article 

    Google Scholar 
    Murata, N., Takahashi, S., Nishiyama, Y. & Allakhverdiev, S. I. Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta Bioenerget. 1767, 414–421 (2007).CAS 
    Article 

    Google Scholar 
    Takahashi, S. & Murata, N. How do environmental stresses accelerate photoinhibition?. Trends Plant Sci. 13, 178–182 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Cumbo, V. R., Baird, A. H. & van Oppen, M. J. H. The promiscuous larvae: Flexibility in the establishment of symbiosis in corals. Coral Reefs 32, 111–120 (2013).ADS 
    Article 

    Google Scholar 
    Little, A. F., Van Oppen, M. J. H. & Willis, B. L. Flexibility in algal endosymbioses shapes growth in reef corals. Science 304, 1492–1494 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Sinniger, F., Morita, R. & Harii, S. ‘Locally extinct’ coral species Seriatopora hystrix found at upper mesophotic depths in Okinawa. Coral Reefs 32, 153 (2013).ADS 
    Article 

    Google Scholar 
    Sinniger, F. et al. Overview of the mesophotic coral ecosystems around Sesoko Island, Okinawa, Japan. Galaxea J. Coral Reef Stud. 24, 69–76 (2022).Article 

    Google Scholar 
    Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131 (2001).Article 

    Google Scholar 
    van Woesik, R., Sakai, K., Ganase, A. & Loya, Y. Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol. Prog. Ser. 434, 67–76 (2011).ADS 
    Article 

    Google Scholar 
    Sinniger, F., Prasetia, R., Yorifuji, M., Bongaerts, P. & Harii, S. Seriatopora diversity preserved in upper mesophotic coral ecosystems in Southern Japan. Front. Mar. Sci. 4, 155 (2017).Article 

    Google Scholar 
    Atoda, K. The larva and postlarval development of some reef-building corals. V. Seriatopora hystrix. Sci. Rep. Tohoku Univ. 19, 33–39 (1951).
    Google Scholar 
    Hata, T. et al. Coral larvae are poor swimmers and require fine-scale reef structure to settle. Sci. Rep. 7, 2249 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Harii, S. & Kayanne, H. Larval dispersal, recruitment, and adult distribution of the brooding stony octocoral Heliopora coerulea on Ishigaki Island, southwest Japan. Coral Reefs 22, 188–196 (2003).Article 

    Google Scholar 
    Mulla, A. J., Lin, C. H., Takahashi, S. & Nozawa, Y. Photo-movement of coral larvae influences vertical positioning in the ocean. Coral Reefs 40, 1297–1306 (2021).Article 

    Google Scholar 
    Figueiredo, J., Baird, A. H., Harii, S. & Connolly, S. R. Increased local retention of reef coral larvae as a result of ocean warming. Nat. Clim. Chang. 4, 498–502 (2014).ADS 
    Article 

    Google Scholar 
    Shanks, A. L., Largier, J., Brink, L., Brubaker, J. & Hooff, R. Demonstration of the onshore transport of larval invertebrates by the shoreward movement of an upwelling front. Limnol. Oceanogr. 45, 230–236 (2000).ADS 
    Article 

    Google Scholar 
    Singh, T. et al. Long-term trends and seasonal variations in environmental conditions in Sesoko Island, Okinawa, Japan. Galaxea J. Coral Reef Stud. 24, 121–133 (2022).Article 

    Google Scholar 
    Roth, M. S., Fan, T.-Y. & Deheyn, D. D. Life history changes in coral fluorescence and the effects of light intensity on larval physiology and settlement in Seriatopora hystrix. PLoS ONE 8, e59476 (2013).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mundy, C. N. & Babcock, R. C. Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement?. J. Exp. Mar. Bio. Ecol. 223, 235–255 (1998).Article 

    Google Scholar 
    Nesa, B., Baird, A. H., Harii, S., Yakovleva, I. & Hidaka, M. Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool. Stud. 51, 12–17 (2012).CAS 

    Google Scholar 
    Cunning, R. & Baker, A. C. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 259–262 (2013).ADS 
    Article 

    Google Scholar 
    Nakamura, T. Mass coral bleaching event in Sekisei lagoon observed in the summer of 2016. J. Jpn. Coral Reef Soc. 19, 29–40 (2017).Article 

    Google Scholar 
    Sakai, K., Singh, T. & Iguchi, A. Bleaching and post-bleaching mortality of Acropora corals on a heat-susceptible reef in 2016. PeerJ 7, e8138 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Edmunds, P. J., Gates, R. D. & Gleason, D. F. The biology of larvae from the reef coral Porites astreoides, and their response to temperature disturbances. Mar. Biol. 139, 981–989 (2001).Article 

    Google Scholar 
    Baker, A. C. Reef corals bleach to survive change. Nature 411, 765–766 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Bongaerts, P. et al. Adaptive divergence in a scleractinian coral: Physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol. Biol. 11, 303 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Einbinder, S. et al. Novel adaptive photosynthetic characteristics of mesophotic symbiotic microalgae within the reef-building coral, Stylophora pistillata. Front. Mar. Sci. 3, 195 (2016).Article 

    Google Scholar 
    Rogers, C. S., Fitz, H. C., Gilnack, M., Beets, J. & Hardin, J. Scleractinian coral recruitment patterns at Salt River submarine canyon, St. Croix, U.S. Virgin Islands. Coral Reefs 3, 69–76 (1984).ADS 
    Article 

    Google Scholar 
    Maida, M., Collb, J. C. & Sammarco, P. W. Shedding new light on scleractinian coral recruitment. J. Exp. Mar. Biol. Ecol. 180, 189–202 (1994).Article 

    Google Scholar 
    Sato, M. Mortality and growth of juvenile coral Pocillopora damicornis (Linnaeus). Coral Reefs 4, 27–33 (1985).ADS 
    Article 

    Google Scholar 
    Nozawa, Y. Micro-crevice structure enhances coral spat survivorship. J. Exp. Mar. Biol. Ecol. 367, 127–130 (2008).Article 

    Google Scholar 
    Gleason, D. F. & Wellington, G. M. Ultraviolet radiation and coral bleaching. Nature 365, 836–838 (1993).ADS 
    Article 

    Google Scholar 
    Shlesinger, T. & Loya, Y. Depth-dependent parental effects create invisible barriers to coral dispersal. Commun. Biol. 4, 1–10 (2021).Article 

    Google Scholar 
    Groves, S. H. et al. Growth rates of Porites astreoides and Orbicella franksi in mesophotic habitats surrounding St. Thomas, US Virgin Islands. Coral Reefs 37, 345–354 (2018).ADS 
    Article 

    Google Scholar 
    Al-Horani, F. A., Al-Moghrabi, S. M. & De Beer, D. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar. Biol. 142, 419–426 (2003).CAS 
    Article 

    Google Scholar 
    Jiang, L. et al. Increased temperature mitigates the effects of ocean acidification on the calcification of juvenile Pocillopora damicornis, but at a cost. Coral Reefs 37, 71–79 (2018).ADS 
    Article 

    Google Scholar 
    Jurriaans, S. & Hoogenboom, M. O. Thermal performance of scleractinian corals along a latitudinal gradient on the Great Barrier Reef. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180546 (2019).CAS 
    Article 

    Google Scholar 
    Brown, B. E. et al. Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18, 99–105 (1999).Article 

    Google Scholar 
    Salih, A., Larkum, A., Cox, G., Kühl, M. & Hoegh-Guldberg, O. Fluorescent pigments in corals are photoprotective. Nature 408, 850–853 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Matz, M. V., Marshall, N. J. & Vorobyev, M. Are corals colorful?. Photochem. Photobiol. 82, 345–350 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    Haddock, S. H. D. & Dunn, C. W. Fluorescent proteins function as a prey attractant: Experimental evidence from the hydromedusa Olindias formosus and other marine organisms. Biol. Open 4, 1094–1104 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eyal, G. et al. Spectral diversity and regulation of coral fluorescence in a mesophotic reef habitat in the Red Sea. PLoS ONE 10, 1–19 (2015).Article 
    CAS 

    Google Scholar 
    Ben-Zvi, O., Eyal, G. & Loya, Y. Light-dependent fluorescence in the coral Galaxea fascicularis. Hydrobiologia 759, 15–26 (2015).Article 

    Google Scholar 
    Roth, M. et al. Fluorescent proteins in dominant mesophotic reef-building corals. Mar. Ecol. Prog. Ser. 521, 63–79 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    Ben-Zvi, O., Eyal, G. & Loya, Y. Response of fluorescence morphs of the mesophotic coral Euphyllia paradivisa to ultra-violet radiation. Sci. Rep. 9, 1–9 (2019).CAS 
    Article 

    Google Scholar 
    Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Nakamura, T., van Woesik, R. & Yamasaki, H. Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar. Ecol. Prog. Ser. 301, 109–118 (2005).ADS 
    Article 

    Google Scholar  More

  • in

    Pupal size as a proxy for fat content in laboratory-reared and field-collected Drosophila species

    Parker, J. & Johnston, L. A. The proximate determinants of insect size. J. Biol. 5, 15 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Honěk, A. Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos 66, 483 (1993).Article 

    Google Scholar 
    Kingsolver, J. G. & Huey, R. B. Size, temperature, and fitness: Three rules. Evol. Ecol. Res. 10, 251–268 (2008).
    Google Scholar 
    Beukeboom, L. W. Size matters in insects—An introduction. Entomol. Exp. Appl. 166, 2–3 (2018).Article 

    Google Scholar 
    West, S. A., Flanagan, K. E. & Godfray, H. C. J. The relationship between parasitoid size and fitness in the field, a study of Achrysocharoides zwoelferi (Hymenoptera: Eulophidae). J. Anim. Ecol. 65, 631–639 (1996).Article 

    Google Scholar 
    Sagarra, L. A., Vincent, C. & Stewart, R. K. Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bull. Entomol. Res. 91, 363–367 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ellers, J., Alphen, J. J. M. V. & Sevenster, J. G. A field study of size–fitness relationships in the parasitoid Asobara tabida. J. Anim. Ecol. 67, 318–324 (1998).Article 

    Google Scholar 
    Armbruster, P. & Hutchinson, R. A. Pupal mass and wing length as indicators of fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). J. Med. Entomol. 39, 699–704 (2002).PubMed 
    Article 

    Google Scholar 
    Tantawy, A. O. & Vetukhiv, M. O. Effects of size on fecundity, longevity and viability in populations of Drosophila pseudoobscura. Am. Nat. 94, 395–403 (1960).Article 

    Google Scholar 
    Lefranc, A. & Bundgaard, J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132, 243–247 (2004).Article 

    Google Scholar 
    Atkinson, D. Temperature and organism size: A biological law for ectotherms? Adv. Ecol. Res. 25, 1–58 (1994).Article 

    Google Scholar 
    Poças, G. M., Crosbie, A. E. & Mirth, C. K. When does diet matter? The roles of larval and adult nutrition in regulating adult size traits in Drosophila melanogaster. J. Insect Physiol. 139, 104051. https://doi.org/10.1016/j.jinsphys.2020.104051 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Tammaru, T. Determination of adult size in a folivorous moth: constraints at instar level? Ecol. Entomol. 23, 80–89 (1998).Article 

    Google Scholar 
    Miller, R. S. & Thomas, J. L. The effects of larval crowding and body size on the longevity of adult Drosophila melanogaster. Ecology 39, 118–125 (1958).Article 

    Google Scholar 
    Nijhout, H. F. The control of body size in insects. Dev. Biol. 261, 1–9 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Shingleton, A. W., Mirth, C. K. & Bates, P. W. Developmental model of static allometry in holometabolous insects. Proc. R. Soc. B 275, 1875–1885 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Koenraadt, C. J. M. Pupal dimensions as predictors of adult size in fitness studies of Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 45, 331–336 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    Stillwell, R. C., Dworkin, I., Shingleton, A. W. & Frankino, W. A. Experimental manipulation of body size to estimate morphological scaling relationships in Drosophila. JoVE 56, 3162. https://doi.org/10.3791/3162 (2011).Article 

    Google Scholar 
    Shin, S.-M., Akram, W. & Lee, J.-J. Effect of body size on energy reserves in Culex pipiens pallens females (Diptera: Culicidae). Entomol. Res. 42, 163–167 (2012).Article 

    Google Scholar 
    Mirth, C. K. & Riddiford, L. M. Size assessment and growth control: How adult size is determined in insects. BioEssays 29, 344–355 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chown, S. L. & Gaston, K. J. Body size variation in insects: A macroecological perspective. Biol. Rev. 85, 139–169 (2010).PubMed 
    Article 

    Google Scholar 
    Beadle, G. W., Tatum, E. L. & Clancy, C. W. Food level in relation to rate of development and eye pigmentation in Drosophila melanogaster. Biol. Bull. 75, 447–462 (1938).Article 

    Google Scholar 
    Gayon, J. History of the concept of allometry1. Am. Zool. 40, 748–758 (2000).
    Google Scholar 
    Takken, W. et al. Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi. Parasit. Vectors 6, 345 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Briegel, H. Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J. Insect Physiol. 36, 165–172 (1990).Article 

    Google Scholar 
    Ellers, J. Fat and eggs: An alternative method to measure the trade-off between survival and reproduction in insect parasitoids. Neth. J. Zool. 3, 227–235 (1996).
    Google Scholar 
    González-Tokman, D. et al. Energy storage, body size and immune response of herbivore beetles at two different elevations in Costa Rica. Rev. Biol. Trop. 67, 608–620 (2019).
    Google Scholar 
    Timmermann, S. E. & Briegel, H. Larval growth and biosynthesis of reserves in mosquitoes. J. Insect Physiol. 45, 461–470 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Strohm, E. Factors affecting body size and fat content in a digger wasp. Oecologia 123, 184–191 (2000).PubMed 
    Article 
    ADS 

    Google Scholar 
    Lease, H. M. & Wolf, B. O. Lipid content of terrestrial arthropods in relation to body size, phylogeny, ontogeny and sex. Physiol. Entomol. 36, 29–38 (2011).CAS 
    Article 

    Google Scholar 
    Arrese, E. L. & Soulages, J. L. Insect fat body: Energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207–225 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kühnlein, R. P. Lipid droplet-based storage fat metabolism in Drosophila. J. Lipid Res. 53, 1430–1436 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Church, R. B. & Robertson, F. W. A biochemical study of the growth of Drosophila melanogaster. J. Exp. Zool. 162, 337–351 (1966).Article 

    Google Scholar 
    Merkey, A. B., Wong, C. K., Hoshizaki, D. K. & Gibbs, A. G. Energetics of metamorphosis in Drosophila melanogaster. J. Insect Physiol. 57, 1437–1445 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nestel, D., Tolmasky, D., Rabossi, A. & Quesada-Allué, L. A. Lipid, carbohydrates and protein patterns during metamorphosis of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 96, 237–244 (2003).CAS 
    Article 

    Google Scholar 
    Lee, K. P. & Jang, T. Exploring the nutritional basis of starvation resistance in Drosophila melanogaster. Funct. Ecol. 28, 1144–1155 (2014).Article 

    Google Scholar 
    Hahn, D. A. & Denlinger, D. L. Meeting the energetic demands of insect diapause: Nutrient storage and utilization. J. Insect Physiol. 53, 760–773 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Tejeda, M. T. et al. Effects of size, sex and teneral resources on the resistance to hydric stress in the tephritid fruit fly Anastrepha ludens. J. Insect Physiol. 70, 73–80 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hoffmann, A. A., Hallas, R., Anderson, A. R. & Telonis-Scott, M. Evidence for a robust sex-specific trade-off between cold resistance and starvation resistance in Drosophila melanogaster. J. Evol. Biol. 18, 804–810 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. Diet effects on honeybee immunocompetence. Biol. Lett. 6, 562–565 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bryk, B., Hahn, K., Cohen, S. M. & Teleman, A. A. MAP4K3 regulates body size and metabolism in Drosophila. Dev. Biol. 344, 150–157 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gasser, M., Kaiser, M., Berrigan, D. & Stearns, S. C. Life-history correlates of evolution under high and low adult mortality. Evolution 54, 1260–1272 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Chippindale, A. K., Chu, T. J. F. & Rose, M. R. Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution 50, 753 (1996).PubMed 
    Article 

    Google Scholar 
    Kristensen, T. N., Overgaard, J., Loeschcke, V. & Mayntz, D. Dietary protein content affects evolution for body size, body fat and viability in Drosophila melanogaster. Biol. Lett. 7, 269–272 (2011).PubMed 
    Article 

    Google Scholar 
    Juarez-Carreño, S. et al. Body-fat sensor triggers ribosome maturation in the steroidogenic gland to initiate sexual maturation in Drosophila. Cell Rep. 37, 109830 (2021).PubMed 
    Article 
    CAS 

    Google Scholar 
    Markow, T. A. The secret lives of Drosophila flies. Elife 4, e06793 (2015).PubMed Central 
    Article 

    Google Scholar 
    Choma, M. A., Suter, M. J., Vakoc, B. J., Bouma, B. E. & Tearney, G. J. Physiological homology between Drosophila melanogaster and vertebrate cardiovascular systems. Dis. Model. Mech. 4, 411–420 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Morgan, T. H., Sturtevant, A. H., Muller, H. J. & Bridges, C. B. The Mechanism of Mendelian Heredity (H. Holt, 1923).
    Google Scholar 
    Dobzhansky, T. The influence of the quantity and quality of chromosomal material on the size of the cells in Drosophila melanogaster. Wilhelm Roux Arch. Entwickl Mech. Org. 115, 363–379 (1929).PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. & Kühnlein, R. P. Drosophila as a model to study obesity and metabolic disease. J. Exp. Biol. 221, 163881 (2018).Article 

    Google Scholar 
    DiAngelo, J. R. & Birnbaum, M. J. Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol. Cell. Biol. 29, 6341–6352 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rovenko, B. M. et al. High sucrose consumption promotes obesity whereas its low consumption induces oxidative stress in Drosophila melanogaster. J. Insect Physiol. 79, 42–54 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hardy, C. M. et al. Obesity-associated cardiac dysfunction in starvation-selected Drosophila melanogaster. Am. J. Physiol.-Regul. Integr. Compar. Physiol. 309, R658–R667 (2015).CAS 
    Article 

    Google Scholar 
    Hardy, C. M. et al. Genome-wide analysis of starvation-selected Drosophila melanogaster—A genetic model of obesity. Mol. Biol. Evol. 35, 50–65 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. et al. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis. Model. Mech. 4, 842–849 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Henry, Y., Renault, D. & Colinet, H. Hormesis-like effect of mild larval crowding on thermotolerance in Drosophila flies. J. Exp. Biol. 221, 169342 (2018).Article 

    Google Scholar 
    Bulletin, E. P. P. O. Drosophila suzukii. EPPO Bull. 43, 417–424 (2013).Article 

    Google Scholar 
    Bächli, G., Vilela, C. R., Escher, S. A. & Saura, A. The Drosophilidae (Diptera) of Fennoscandia and Denmark (Brill Academic Publishers, 2004).Book 

    Google Scholar 
    Markow, T. A. & O’Grady, P. M. Drosophila: A Guide to Species Identification and Use (Elsevier, 2006).
    Google Scholar 
    Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Visser, B. et al. Variation in lipid synthesis, but genetic homogeneity, among Leptopilina parasitic wasp populations. Ecol. Evol. 8, 7355–7364 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Williams, C. M., Thomas, R. H., MacMillan, H. A., Marshall, K. E. & Sinclair, B. J. Triacylglyceride measurement in small quantities of homogenised insect tissue: Comparisons and caveats. J. Insect Physiol. 57, 1602–1613 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2020).Fox, J. & Weisberg, S. An R Companion to Applied Regression 2nd edn. (Sage, 2011).
    Google Scholar 
    Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M. Emmeans: Estimated marginal means, aka least-squares means. R Package Version 1, 3 (2018).
    Google Scholar 
    Burnham, K. P. & Anderson, D. R. A practical information-theoretic approach. In Model Selection and Multimodel Inference (ed. Burnham, K. P.) (Springer, 2002).MATH 

    Google Scholar 
    Crawley, M. J. The R Book (Wiley, 2007).MATH 
    Book 

    Google Scholar 
    Borash, D. J. & Ho, G. T. Patterns of selection: Stress resistance and energy storage in density-dependent populations of Drosophila melanogaster. J. Insect Physiol. 47, 1349–1356 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    Klepsatel, P., Procházka, E. & Gáliková, M. Crowding of Drosophila larvae affects lifespan and other life-history traits via reduced availability of dietary yeast. Exp. Gerontol. 110, 298–308 (2018).PubMed 
    Article 

    Google Scholar 
    Henry, Y., Overgaard, J. & Colinet, H. Dietary nutrient balance shapes phenotypic traits of Drosophila melanogaster in interaction with gut microbiota. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 241, 110626 (2020).CAS 
    Article 

    Google Scholar 
    Ireland, S. & Turner, B. The effects of larval crowding and food type on the size and development of the blowfly, Calliphora vomitoria. Forensic Sci. Int. 159, 175–181 (2006).PubMed 
    Article 

    Google Scholar 
    Saunders, D. S. & Bee, A. Effects of larval crowding on size and fecundity of the blow fly, Calliphora vicina (Diptera: Calliphoridae). EJE 92, 615–622 (2013).
    Google Scholar 
    Ziegler, R. Changes in lipid and carbohydrate metabolism during starvation in adult Manduca sexta. J. Comp. Physiol. B 161, 125–131 (1991).CAS 
    PubMed 
    Article 

    Google Scholar 
    Ojeda-Avila, T., Arthur Woods, H. & Raguso, R. A. Effects of dietary variation on growth, composition, and maturation of Manduca sexta (Sphingidae: Lepidoptera). J. Insect Physiol. 49, 293–306 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Borash, D. J., Gibbs, A. G., Joshi, A. & Mueller, L. D. A genetic polymorphism maintained by natural selection in a temporally varying environment. Am. Nat. 151, 148. https://doi.org/10.1086/286108 (1998).CAS 
    Article 
    PubMed 

    Google Scholar 
    Klepsatel, P., Knoblochová, D., Girish, T. N., Dircksen, H. & Gáliková, M. The influence of developmental diet on reproduction and metabolism in Drosophila. BMC Evol. Biol. 20, 93 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Matzkin, L. M., Johnson, S., Paight, C., Bozinovic, G. & Markow, T. A. Dietary protein and sugar differentially affect development and metabolic pools in ecologically diverse Drosophila. J. Nutr. 141, 1127–1133 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Musselman, L. P. et al. Role of fat body lipogenesis in protection against the effects of caloric overload in Drosophila. J. Biol. Chem. 288, 8028–8042 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Reeve, M. W., Fowler, K. & Partridge, L. Increased body size confers greater fitness at lower experimental temperature in male Drosophila melanogaster. J. Evol. Biol. 13, 836–844 (2000).Article 

    Google Scholar 
    Lounibos, L. P. et al. Does temperature affect the outcome of larval competition between Aedes aegypti and Aedes albopictus?. J. Vector Ecol. 27, 86–95 (2002).CAS 
    PubMed 

    Google Scholar 
    Bergland, A. O., Genissel, A., Nuzhdin, S. V. & Tatar, M. Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 180, 567–582 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Holm, S. et al. A comparative perspective on longevity: The effect of body size dominates over ecology in moths. J. Evol. Biol. 29, 2422–2435 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    Nunney, L. The response to selection for fast larval development in Drosophila melanogaster and its effect on adult weight: An example of a fitness trade-off. Evolution 50, 1193–1204 (1996).PubMed 
    Article 

    Google Scholar 
    Partridge, L. & Farquhar, M. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anim. Behav. 31, 871–877 (1983).Article 

    Google Scholar 
    Markow, T. A. & Ricker, J. P. Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69, 122–127 (1992).PubMed 
    Article 

    Google Scholar 
    Wikelski, M. & Romero, L. M. Body size, performance and fitness in galapagos marine iguanas. Integr. Comp. Biol. 43, 376–386 (2003).PubMed 
    Article 

    Google Scholar 
    van Buskirk, J. & Crowder, L. B. Life-history variation in marine turtles. Copeia 1994, 66–81 (1994).Article 

    Google Scholar 
    Broderick, A. C., Glen, F., Godley, B. J. & Hays, G. C. Variation in reproductive output of marine turtles. J. Exp. Mar. Biol. Ecol. 288, 95–109 (2003).Article 

    Google Scholar 
    Wauters, L. A. et al. Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30, 51–65 (2007).Article 

    Google Scholar 
    Lindström, J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343–348 (1999).PubMed 
    Article 

    Google Scholar 
    Reim, C., Teuschl, Y. & Blanckenhorn, W. U. Size-dependent effects of temperature and food stress on energy reserves and starvation resistance in yellow dung flies. Evol. Ecol. Res. 8, 1215–1234 (2006).
    Google Scholar 
    Kölliker-Ott, U. M., Blows, M. W. & Hoffmann, A. A. Are wing size, wing shape and asymmetry related to field fitness of Trichogramma egg parasitoids? Oikos 100, 563–573 (2003).Article 

    Google Scholar 
    Knapp, M. Relative importance of sex, pre-starvation body mass and structural body size in the determination of exceptional starvation resistance of Anchomenus dorsalis (Coleoptera: Carabidae). PLoS ONE 11, e0151459 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Lue, C.-H. et al. DROP: Molecular voucher database for identification of Drosophila parasitoids. Mol. Ecol. Resour. 21, 2437–2454 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Visser, B. et al. Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle. Proc. Natl. Acad. Sci. 107, 8677–8682 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    Visser B et al. Why do
    many parasitoids lack adult triglyceride accumulation, despite functioning fatty acid biosynthesis machinery? EcoEvoRxiv:
    https://doi.org/10.32942/osf.io/zpf4jArakawa, R., Miura, M. & Fujita, M. Effects of host species on the body size, fecundity, and longevity of Trissolcus mitsukurii (Hymenoptera: Scelionidae), a solitary egg parasitoid of stink bugs. Appl. Entomol. Zool. 39, 177–181 (2004).Article 

    Google Scholar 
    Visser, B., Alborn, H.T., Rondeaux, S. et al. Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic
    wasps. Sci Rep 11, 7751 (2021). https://doi.org/10.1038/s41598-021-86736-8.Krüger, A. P. et al. Effects of irradiation dose on sterility induction and quality parameters of Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol. 111, 741–746 (2018).PubMed 
    Article 

    Google Scholar 
    Nikolouli, K. et al. Sterile insect technique and Wolbachia symbiosis as potential tools for the control of the invasive species Drosophila suzukii. J. Pest Sci. 91, 1–15 (2017).
    Google Scholar 
    Nikolouli, K., Sassù, F., Mouton, L., Stauffer, C. & Bourtzis, K. Combining sterile and incompatible insect techniques for the population suppression of Drosophila suzukii. J. Pest Sci. 93, 647–661 (2020).CAS 
    Article 

    Google Scholar 
    Calkins, C. O. & Parker, A. G. Sterile insect quality. In Sterile Insect Technique (eds Dyck, V. A. et al.) 269–296 (Springer, 2005).Chapter 

    Google Scholar  More