More stories

  • in

    Reproductive characteristics of American bullfrogs (Lithobates catesbeianus) in their invasive range of the Pacific Northwest, USA

    1.
    Elton, C. The Ecology of Invasions by Animals and Plants (Methuen, London, 1958).
    Google Scholar 
    2.
    Simberloff, D. Invasive Species: What Everyone Needs to Know (Oxford University Press, Oxford, 2013).
    Google Scholar 

    3.
    Ehrenfeld, J. G. Ecosystem consequences of biological invasions. Annu. Rev. Ecol. Evol. Syst. 41, 59–80 (2010).
    Article  Google Scholar 

    4.
    Simberloff, D. How common are invasion-induced ecosystem impacts?. Biol. Invasions 13, 1255–1268 (2011).
    Article  Google Scholar 

    5.
    Simberloff, D. Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both?. Ecol. Lett. 9, 912–919 (2006).
    PubMed  Article  Google Scholar 

    6.
    Fukami, T. et al. Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol. Lett. 9, 1299–1307 (2006).
    PubMed  Article  Google Scholar 

    7.
    Gibbons, J. W. et al. The global decline of reptiles Deja Vu amphibians. Bioscience 50, 653–666 (2000).
    Article  Google Scholar 

    8.
    Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L. & Gaston, K. J. Avian extinction and mammalian introductions on oceanic islands. Science 305, 1955 (2004).
    ADS  PubMed  Article  CAS  Google Scholar 

    9.
    Paini, D. R. et al. Global threat to agriculture from invasive species. Proc. Natl. Acad. Sci. 113, 7575–7579 (2016).
    PubMed  Article  CAS  Google Scholar 

    10.
    Juliano, S. A. & Lounibos, L. P. Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol. Lett. 8, 558–574 (2005).
    PubMed  PubMed Central  Article  Google Scholar 

    11.
    Pimentel, D., Lach, L., Zuniga, R. & Morrison, D. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65 (2000).
    Article  Google Scholar 

    12.
    Rogers, W. E. Invasive species. In Reference Module Earth Systems and Environmental Sciences (ed. Flow, E. S.) (Elsevier, Amsterdam, 2017).
    Google Scholar 

    13.
    Booth, B. D., Murphy, S. D. & Swanton, C. J. Weed Ecology in Natural and Agricultural Systems (CABI publishing, Wallingford, 2003).
    Google Scholar 

    14.
    White, E. M., Wilson, J. C. & Clarke, A. R. Biotic indirect effects: a neglected concept in invasion biology. Divers. Distrib. 12, 443–455 (2006).
    Article  Google Scholar 

    15.
    Hui, C. et al. Defining invasiveness and invasibility in ecological networks. Biol. Invasions 18, 971–983 (2016).
    Article  Google Scholar 

    16.
    Ricciardi, A., Hoopes, M. F., Marchetti, M. P. & Lockwood, J. L. Progress toward understanding the ecological impacts of nonnative species. Ecol. Monogr. 83, 263–282 (2013).
    Article  Google Scholar 

    17.
    Kolar, C. S. & Lodge, D. M. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204 (2001).
    PubMed  Article  Google Scholar 

    18.
    Lodge, D. M. Biological invasions: lessons for ecology. Trends Ecol. Evol. 8, 133–137 (1993).
    PubMed  Article  CAS  Google Scholar 

    19.
    Savidge, J. A., Qualls, F. J. & Rodda, G. H. Reproductive biology of the brown tree snake, Boiga irregularis (Reptilia: Colubridae), during colonization of Guam and comparison with that in their native range. Pac. Sci. 61, 191–199 (2007).
    Article  Google Scholar 

    20.
    Gardner, P. G., Frazer, T. K., Jacoby, C. A. & Yanong, R. P. E. Reproductive biology of invasive lionfish (Pterois spp.). Front. Mar. Sci. 2, 7 (2015).
    Article  Google Scholar 

    21.
    Van Kleunen, M., Dawson, W., Schlaepfer, D., Jeschke, J. M. & Fischer, M. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol. Lett. 13, 947–958 (2010).
    PubMed  Google Scholar 

    22.
    Barnosky, A. D. et al. Has the Earth/’s sixth mass extinction already arrived?. Nature 471, 51–57 (2011).
    ADS  PubMed  Article  CAS  Google Scholar 

    23.
    Ceballos, G. et al. Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253 (2015).
    ADS  PubMed  PubMed Central  Article  Google Scholar 

    24.
    Measey, G. J. et al. Ongoing invasions of the African clawed frog, Xenopus laevis: a global review. Biol. Invasions 14, 2255–2270 (2012).
    Article  Google Scholar 

    25.
    Bucciarelli, G. M., Blaustein, A. R., Garcia, T. S. & Kats, L. B. Invasion complexities: the diverse impacts of nonnative species on amphibians. Copeia 2014, 611–632 (2014).
    Article  Google Scholar 

    26.
    Measey, G. J. et al. A global assessment of alien amphibian impacts in a formal framework. Divers. Distrib. 22, 970–981 (2016).
    Article  Google Scholar 

    27.
    Kumschick, S. et al. Impact assessment with different scoring tools: how well do alien amphibian assessments match?. NeoBiota 33, 53–66 (2017).
    Article  Google Scholar 

    28.
    Kraus, F. Impacts from invasive reptiles and amphibians. Annu. Rev. Ecol. Evol. Syst. 46, 75–97 (2015).
    Article  Google Scholar 

    29.
    Selechnik, D., Rollins, L. A., Brown, G. P., Kelehear, C. & Shine, R. The things they carried: the pathogenic effects of old and new parasites following the intercontinental invasion of the Australian cane toad (Rhinella marina). Int. J. Parasitol. Parasites Wildl. 6, 375–385 (2017).
    PubMed  Article  CAS  Google Scholar 

    30.
    Shine, R. Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol. Appl. 5, 107–116 (2012).
    PubMed  Article  Google Scholar 

    31.
    Adams, M. J. & Pearl, C. A. Problems and opportunities managing invasive bullfrogs: is there any hope? In Biological Invaders in Inland Waters: Profiles, Distribution, and Threats (ed. Gherardi, F.) 679–693 (Springer, Dordrecht, 2007).
    Google Scholar 

    32.
    Pili, A. N., Supsup, C. E., Sy, E. Y., Diesmos, M. L. L. & Diesmos, A. C. Spatial dynamics of invasion and distribution of alien frogs in a biodiversity hotspot archipelago. In Island Invasives: Scaling Up to Meet the Challenge 337–347 (IUCN, 2019).

    33.
    Pearl, C., Adams, M., Leuthold, N. & Bury, R. Amphibian occurrence and aquatic invaders in a changing landscape: implications for wetland mitigation in the Willamette valley, Oregon, USA. Wetlands 25, 76–88 (2005).
    Article  Google Scholar 

    34.
    Govindarajulu, P., Price, W. M. S. & Anholt, B. R. Introduced bullfrogs (Rana catesbeiana) in western Canada: has their ecology diverged?. J. Herpetol. 40, 249–260 (2006).
    Article  Google Scholar 

    35.
    Bai, C., Liu, X., Fisher, M. C., Garner, T. W. J. & Li, Y. Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Divers. Distrib. 18, 307–318 (2012).
    Article  Google Scholar 

    36.
    Rago, A., While, G. M. & Uller, T. Introduction pathway and climate trump ecology and life history as predictors of establishment success in alien frogs and toads. Ecol. Evol. 2, 1437–1445 (2012).
    PubMed  PubMed Central  Article  Google Scholar 

    37.
    Xuan, L., Yiming, L. & McGarrity, M. Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China. Biol. Invasions 12, 2037–2047 (2010).
    Article  Google Scholar 

    38.
    Both, C. et al. Widespread occurrence of the American Bullfrog, Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae) Brazil. South Am. J. Herpetol. 6, 127–134 (2011).
    Article  Google Scholar 

    39.
    Bøhn, T., Terje Sandlund, O., Amundsen, P.-A. & Primicerio, R. Rapidly changing life history during invasion. Oikos 106, 138–150 (2004).
    Article  Google Scholar 

    40.
    Lima, S. L., Costa, C. L. S., Agostinho, C. A., Andrade, D. R. & Pereira, H. P. Estimate of bullfrog size at first sexual maturation, Rana catesbeiana, in the intensive growing Anfigranja system. Rev. Bras. Zootec. Braz. J. Anim. Sci. 27, 416–420 (1998).
    Google Scholar 

    41.
    Leivas, P. T., Moura, M. O. & Favaro, L. F. The reproductive biology of the invasive Lithobates catesbeianus (Amphibia:Anura). J. Herpetol. 46, 153–161 (2012).
    Article  Google Scholar 

    42.
    Bruneau, M. & Magnin, E. Croissance, nutrition et reproduction des ouaouarons Rana catesbeiana Shaw (Amphibia Anura) des Laurentides au nord de Montreal. Can. J. Zool. 58, 175–183 (1980).
    Article  Google Scholar 

    43.
    Shirose, L. J., Brooks, R. J., Barta, J. R. & Desser, S. S. Intersexual differences in growth, mortality, and size at maturity in bullfrogs in central Ontario. Can. J. Zool. 71, 2363–2369 (1993).
    Article  Google Scholar 

    44.
    Jennings, M. R. & Hayes, M. P. Pre-1900 overharvest of California red-legged frogs (Rana aurora draytonii): the inducement for Bullfrog (Rana catesbeiana) introduction. Herpetologica 41, 94–103 (1985).
    Google Scholar 

    45.
    Guariento, R. D., Carneiro, L. S., Jorge, J. S. & Caliman, A. Assessing the risk effects of native predators on the exotic American bullfrog (Lithobates catesbeianus) and their indirect consequences to ecosystem function. Acta Oecologica 91, 50–56 (2018).
    ADS  Article  Google Scholar 

    46.
    Crump, M. L. & Scott, N. J. Jr. Chapter 2. Visual encounter surveys. In Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians (eds Heyer, W. R. et al.) 84–92 (Smithsonian Institution Press, Washington, 1994).
    Google Scholar 

    47.
    Browne, R. K. & Zippel, K. Reproduction and larval rearing of amphibians. ILAR J. 48, 214–234 (2007).
    PubMed  Article  CAS  Google Scholar 

    48.
    Costa, C. L. S., Lima, S. L., Andrade, D. R. & Agostinho, C. A. Morphological characterization of development stages of male reproduction apparel of bullfrog, Rana catesbeiana, in the intensive Anfigranja system. Rev. Bras. Zootec. Braz. J. Anim. Sci. 27, 651–657 (1998).
    Google Scholar 

    49.
    Costa, C. L. S., Lima, S. L., Andrade, D. R. & Agostinho, C. A. Morphological characterization of the development stages of female reproduction apparel of bullfrog, Rana catesbeiana, in the intensive Anfigranja systems. Rev. Bras. Zootec. Braz. J. Anim. Sci. 27, 642–650 (1998).
    Google Scholar 

    50.
    Kaefer, I. L., Boelter, R. A. & Cechin, S. Z. Reproductive biology of the invasive bullfrog Lithobates catesbeianus in southern Brazil. Ann. Zool. Fenn. 44, 435–444 (2007).
    Google Scholar 

    51.
    Howard, R. D. Sexual dimorphism in bullfrogs. Ecology 62, 303–310 (1981).
    Article  Google Scholar 

    52.
    Jones, L. L. C., Leonard, W. P. & Olson, D. H. Amphibians of the Pacific Northwest (Seattle Audubon Society, Seattle, 2005).
    Google Scholar 

    53.
    Nussbaum, R. A., Brodie, E. D. & Storm, R. M. Amphibians and Reptiles of the Pacific Northwest (University Press of Idaho, Moscow, 1983).
    Google Scholar 

    54.
    Govindarajulu, P., Altwegg, R. & Anholt, B. R. Matrix model investigation of invasive species control: bullfrogs on Vancouver Island. Ecol. Appl. 15, 2161–2170 (2005).
    Article  Google Scholar 

    55.
    Cook, M. T., Heppell, S. S. & Garcia, T. S. Invasive bullfrog larvae lack developmental plasticity to changing hydroperiod. J. Wildl. Manag. 77, 655–662 (2013).
    Article  Google Scholar 

    56.
    Jennette, M. A., Snodgrass, J. W. & Forester, D. C. Variation in age, body size, and reproductive traits among urban and rural amphibian populations. Urban Ecosyst. 22, 137–147 (2019).
    Article  Google Scholar 

    57.
    Bredeweg, E. M., Urbina, J., Morzillo, A. T. & Garcia, T. S. Starting on the right foot: carryover effects of larval hydroperiod and terrain moisture on post-metamorphic frog movement behavior. Front. Ecol. Evol. 7, 97 (2019).
    Article  Google Scholar 

    58.
    Burton, O. J., Phillips, B. L. & Travis, J. M. J. Trade-offs and the evolution of life-histories during range expansion. Ecol. Lett. 13, 1210–1220 (2010).
    PubMed  Article  Google Scholar 

    59.
    Chuang, A. & Peterson, C. R. Expanding population edges: theories, traits, and trade-offs. Glob. Change Biol. 22, 494–512 (2016).
    ADS  Article  Google Scholar 

    60.
    Kelehear, C. & Shine, R. Tradeoffs between dispersal and reproduction at an invasion front of cane toads in tropical Australia. Sci. Rep. 10, 486 (2020).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    61.
    Hudson, C. M., Phillips, B. L., Brown, G. P. & Shine, R. Virgins in the vanguard: low reproductive frequency in invasion-front cane toads. Biol. J. Linn. Soc. 116, 743–747 (2015).
    Article  Google Scholar 

    62.
    Courant, J., Secondi, J., Bereiziat, V. & Herrel, A. Resources allocated to reproduction decrease at the range edge of an expanding population of an invasive amphibian. Biol. J. Linn. Soc. 122, 157–165 (2017).
    Article  Google Scholar 

    63.
    Vimercati, G., Davies, S. J. & Measey, J. Invasive toads adopt marked capital breeding when introduced to a cooler, more seasonal environment. Biol. J. Linn. Soc. 128, 657–671 (2019).
    Article  Google Scholar 

    64.
    Sol, D. et al. Unraveling the life history of successful invaders. Science 337, 580 (2012).
    ADS  PubMed  Article  CAS  PubMed Central  Google Scholar 

    65.
    Descamps, S. & De Vocht, A. The sterile male release approach as a method to control invasive amphibian populations: a preliminary study on Lithobates catesbeianus. Manag. Biol. Invasions 8, 361–370 (2017).
    Article  Google Scholar 

    66.
    McCoid, M. J. & Fritts, T. H. Growth and fatbody cycles in feral populations of the African clawed frog, Xenopus laevis (Pipidae), in California with comments on reproduction. Southwest. Nat. 34, 499–505 (1989).
    Article  Google Scholar 

    67.
    Werner, E. E. Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am. Nat. 128, 319–341 (1986).
    Article  Google Scholar 

    68.
    Howard, R. D. Sexual selection and variation in reproductive success in a long-lived organism. Am. Nat. 122, 301–325 (1983).
    ADS  Article  Google Scholar 

    69.
    Emlen, S. T. ‘Double clutching’ and its possible significance in the bullfrog. Copeia 1977, 749–751 (1977).
    Article  Google Scholar 

    70.
    Kiesecker, J. M. & Blaustein, A. R. Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red-legged frogs (Rana aurora). Conserv. Biol. 12, 776–787 (1998).
    Article  Google Scholar 

    71.
    Blaustein, A. R. & Kiesecker, J. M. Complexity in conservation: lessons from the global decline of amphibian populations. Ecol. Lett. 5, 597–608 (2002).
    Article  Google Scholar 

    72.
    Rowe, J. C. et al. Disentangling effects of invasive species and habitat while accounting for observer error in a long-term amphibian study. Ecosphere 10, e02674 (2019).
    Article  Google Scholar 

    73.
    Sharifian-Fard, M. et al. Ranavirosis in invasive bullfrogs Belgium. Emerg. Infect. Dis. 17, 2371–2372 (2011).
    PubMed  PubMed Central  Article  Google Scholar 

    74.
    Gervasi, S. S. et al. Experimental evidence for American bullfrog (Lithobates catesbeianus) susceptibility to chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 10, 166–171 (2013).
    PubMed  Article  Google Scholar 

    75.
    Martel, A. et al. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Natl. Acad. Sci. 110, 15325 (2013).
    ADS  PubMed  Article  Google Scholar 

    76.
    Urbina, J., Bredeweg, E. M., Garcia, T. S. & Blaustein, A. R. Host-pathogen dynamics among the invasive American bullfrog (Lithobates catesbeianus) and chytrid fungus (Batrachochytrium dendrobatidis). Hydrobiologia 817, 267–277 (2018).
    Article  CAS  Google Scholar 

    77.
    Ficetola, G. F. et al. Pattern of distribution of the American bullfrog Rana catesbeiana in Europe. Biol. Invasions 9, 767–772 (2007).
    Article  Google Scholar 

    78.
    Ryan, M. J. The reproductive behavior of the bullfrog (Rana catesbeiana). Copeia 1980, 108–114 (1980).
    Article  Google Scholar 

    79.
    Willis, Y. L., Moyle, D. L. & Baskett, T. S. Emergence, breeding, hibernation, movements and transformation of the bullfrog, Rana catesbeiana Missouri. Copeia 1956, 30–41 (1956).
    Article  Google Scholar 

    80.
    Wright, A. & Wright, A. Handbook of Frogs and Toads of the United States and Canada (Comstock, London, 1949).
    Google Scholar 

    81.
    Raney, E. C. & Ingram, W. M. Growth of tagged frogs (Rana catesbeiana Shaw and Rana clamitans Daudin) under natural conditions. Am. Midl. Nat. 26, 201–206 (1941).
    Article  Google Scholar 

    82.
    George, I. A study of the bullfrog, Rana catesbeiana Shaw, at Baton Rouge, Louisiana (University of Michigan, Ann Arbor, 1940).
    Google Scholar 

    83.
    Wright, A. Frogs: Their Natural History and Utilization. Series: Document (Bureau of Fisheries, United States) no. 888. (Govt. Print. Off, Washington, 1920). More

  • in

    Ancient dog diets on the Pacific Northwest Coast: zooarchaeological and stable isotope modelling evidence from Tseshaht territory and beyond

    1.
    Moss, M. L. Northwest Coast: Archaeology as Deep History (Society for American Archaeology Press, Washington, 2011).
    Google Scholar 
    2.
    McKechnie, I., Moss, M. L. & Crockford, S. J. Dogs and other canids of the northwest coast of North America: animal husbandry in a region without agriculture?. J. Anthrop. Archaeol https://doi.org/10.1016/j.jaa.2020.101209 (2020).
    Article  Google Scholar 

    3.
    Crockford, S. J. Osteometry of Makah and Coast Salish Dogs (Archaeology Press, Simon Fraser University, Burnaby, 1997).
    Google Scholar 

    4.
    Crockford, S. J. A Practical Guide to In Situ Dog Remains for the Field Archaeologist (Pacific Identifications Inc., Berlin, 2009).
    Google Scholar 

    5.
    Guiry, E. J. Dogs as analogs in stable isotope-based human paleodietary reconstructions: a review and considerations for future use. J. Arch. Methods Theory 19, 351–376 (2012).
    Article  Google Scholar 

    6.
    Burleigh, R. & Brothwell, D. Studies on Amerindian dogs, 1: carbon isotopes in relation to maize in the diet of domestic dogs from early Peru and Ecuador. J. Archaeol. Sci. 5, 355–362 (1978).
    CAS  Article  Google Scholar 

    7.
    Cannon, A., Schwarcz, H. P. & Knyf, M. Marine-based subsistence trends and the stable isotope analysis of dog bones from Namu, British Columbia. J. Archaeol. Sci. 26, 399–407 (1999).
    Article  Google Scholar 

    8.
    Chisholm, B. S., Nelson, D. E. & Schwarcz, H. P. Stable carbon isotope ratios as a measure of marine versus terrestrial protein in ancient diets. Science 216, 1131–1132 (1982).
    ADS  CAS  PubMed  Article  Google Scholar 

    9.
    DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341–351 (1981).
    ADS  CAS  Article  Google Scholar 

    10.
    Schoeninger, M. J. & DeNiro, M. J. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim. Cosmochim. Acta 48, 625–639 (1984).
    ADS  CAS  Article  Google Scholar 

    11.
    Guiry, E. J. A canine surrogacy approach to human paleodietary bone chemistry: past development and future directions. Arch. Anthropol. Sci. 5, 275–286 (2013).
    Article  Google Scholar 

    12.
    Guiry, E. J. & Grimes, V. Domestic dog (Canis familiaris) diets among coastal Late Archaic groups of northeastern North America: a case study for the canine surrogacy approach. J. Anthrop. Archaeol. 32, 732–745 (2013).
    Article  Google Scholar 

    13.
    Grier, C. Affluence on the prehistoric northwest coast of North America. In: Beyond ‘Affluent-Foragers’: Rethinking Hunter-Gatherer Complexity. Proceedings of the 9th ICAZ Conference, Durham 2002 (eds Grier, C., Kim, J. & Uchiyama, J.) 126–135 (Oxbow Books, 2006).

    14.
    Ames, K. M. et al. Stable isotope and ancient DNA analysis of dog remains from Cathlapotle (45CL1), a contact-era site on the Lower Columbia River. J. Archaeol. Sci. 57, 268–282 (2015).
    CAS  Article  Google Scholar 

    15.
    Tifental, E. The Bridge River Dogs: Interpreting aDNA and Stable Isotope Analysis Collected from Dog Remains. MA Thesis, University of Montana (2016).

    16.
    Barta, J. L. Addressing Issues of Domestication and Cultural Continuity on the Northwest Coast Using Ancient DNA and Dogs. PhD Dissertation, McMaster University (2006).

    17.
    Guiry, E. et al. Differentiating salmonid migratory ecotypes through stable isotope analysis of collagen: archaeological and ecological applications. PLoS ONE 15, e0232180. https://doi.org/10.1371/journal.pone.0232180 (2020).
    CAS  Article  PubMed  PubMed Central  Google Scholar 

    18.
    Lovell, N. C., Chisholm, B. S., Nelson, D. E. & Schwarcz, H. P. Prehistoric salmon consumption in interior British Columbia. Can. J. Archaeol. 10, 99–106 (1986).
    Google Scholar 

    19.
    Szpak, P., Orchard, T. J. & Gröcke, D. R. A late holocene vertebrate food web from southern Haida Gwaii (Queen Charlotte Islands, British Columbia). J. Archaeol. Sci. 36, 2734–2741 (2009).
    Article  Google Scholar 

    20.
    Stock, B. C. & Semmens, B. X. MixSIAR GUI User Manual, Version 1.0. https://conserver.iugo-cafe.org/user/brice.semmens/MixSIR (2013).

    21.
    Drucker, P. The Northern and Central Nootkan Tribes, Vol. 144 (Smithsonian Institution, Washington, 1951).
    Google Scholar 

    22.
    Dierks, K. Osteobiography of an Ancient Nuu-chah-nulth Woolly Dog: Investigating the Life and Death of a Domestic Dog from Tseshaht Territory in Barkley Sound. Honours Thesis, University of Victoria (2020).

    23.
    McKechnie, I. An Archaeology of Food and Settlement on the Northwest Coast. PhD Dissertation, University of British Columbia (2014).

    24.
    MacLean, K. An Analysis of the Flaked Stone Assemblage from the Hiikwis Site Complex, Barkley Sound, British Columbia. MA Thesis, University of Victoria (2012).

    25.
    Smith, N. F., McKechnie, I. & St. Claire, D. E. Kakmakimilh–Keith Island Wharf and Gazebo Installation: An Archaeological Impact Assessment (Report Prepared for Tseshaht First Nation and Pacific Rim National Park Reserve of Canada, 2012).

    26.
    Guiry, E. J., Szpak, P. & Richards, M. P. Effects of lipid extraction and ultrafiltration on stable carbon and nitrogen isotopic compositions of fish bone collagen. Rapid Commun. Mass Spectrom. 30, 1591–1600 (2016).
    ADS  CAS  PubMed  Article  Google Scholar 

    27.
    Guiry, E. J. et al. Lake Ontario salmon (Salmo salar) were not migratory: a long-standing historical debate solved through stable isotope analysis. Sci. Rep. 6, 36249 (2016).
    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

    28.
    Szpak, P., Metcalfe, J. Z. & Macdonald, R. A. Best practices for calibrating and reporting stable isotope measurements in archaeology. J. Archaeol. Sci. Rep. 13, 609–616 (2017).
    Google Scholar 

    29.
    Ambrose, S. H. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 17, 431–451 (1990).
    Article  Google Scholar 

    30.
    Alter, S. E., Newsome, S. D. & Palumbi, S. R. Pre-whaling genetic diversity and population ecology in eastern Pacific gray whales: insights from ancient DNA and stable isotopes. PLoS ONE 7, e35039 (2012).
    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

    31.
    Newsome, S. D. et al. The shifting baseline of northern fur seal ecology in the northeast Pacific Ocean. PNAS 104, 9709–9714 (2007).
    ADS  CAS  PubMed  Article  Google Scholar 

    32.
    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 

    33.
    Bocherens, H. & Drucker, D. Trophic level isotopic enrichment of carbon and nitrogen in bone collagen: case studies from recent and ancient terrestrial ecosystems. Int. J. Osteoarchaeol. 13, 46–53 (2003).
    Article  Google Scholar 

    34.
    Szepanski, M. M., Ben-David, M. & Van Ballenberghe, V. Assessment of anadromous salmon resources in the diet of the Alexander Archipelago wolf using stable isotope analysis. Oecologia 120, 327–335 (1999).
    ADS  CAS  PubMed  Article  Google Scholar 

    35.
    Szpak, P., Orchard, T. J., McKechnie, I. & Gröcke, D. R. Historical ecology of late Holocene sea Otters (Enhydra lutris) from northern British Columbia: isotopic and zooarchaeological perspectives. J. Archaeol. Sci. 39, 1553–1571. https://doi.org/10.1016/j.jas.2011.12.006 (2012).
    Article  Google Scholar 

    36.
    Markel, R. W. Rockfish Recruitment and Trophic Dynamics on the West Coast of Vancouver Island: Fishing, Ocean Climate, and Sea Otters. PhD Dissertation, University of British Columbia (2011).

    37.
    McKechnie, I. & Wigen, R. J. Toward a historical ecology of pinniped and sea otter hunting traditions on the Coast of Southern British Columbia. In Human Impacts on Seals, Sea Lions, and Sea Otters: Integrating Archaeology and Ecology in the Northeast Pacific (eds Braje, T. J. & Rick, T. C.) 129–166 (Univ. of California, Oakland, 2011).
    Google Scholar 

    38.
    McMillan, A. D., McKechnie, I., St. Claire, D. E. & Frederick, S. G. Exploring variability in maritime resource use on the Northwest Coast: a case study from Barkley Sound, Western Vancouver Island. Can. J. Archaeol. 32, 214–238 (2008).
    Google Scholar 

    39.
    Westre, N. J. Vertebrate Faunal Analysis of the Hiikwis Site Complex (DfSh-15 and DfSh-16) in Barkley Sound, British Columbia. MA Thesis, University of Victoria (2014).

    40.
    Wigen, R. J. Faunal analysis for Kakmakimilh, Keith Island, 306T (DfSh-17) In Kakmakimilh–Keith Island Wharf and Gazebo Installation: An Archaeological Impact Assessment (eds Smith, N. F., McKechnie, I. & St. Claire, D. E.) (Report Prepared by for Tseshaht First Nation and Pacific Rim National Park Reserve of Canada, 2013).

    41.
    Newsome, S. D., Martinez del Rio, C., Bearhop, S. & Phillips, D. L. A niche for isotopic ecology. Front. Ecol. Environ. 5, 429–443 (2007).
    Article  Google Scholar 

    42.
    Ramshaw, B. C., Pakhomov, E. A., Markel, R. W. & Kaehler, S. Quantifying spatial and temporal variations in phytoplankton and kelp isotopic signatures to estimate the distribution of kelp-derived detritus off the west coast of Vancouver Island, Canada. Limnol. Oceanogr. https://doi.org/10.1002/lno.10555 (2017).
    Article  Google Scholar 

    43.
    Zanden, M. J. V. & Fetzer, W. W. Global patterns of aquatic food chain length. Oikos 116, 1378–1388 (2007).
    Article  Google Scholar 

    44.
    Diaz, A. L. Resource Relationships Along the Fraser River: A Stable Isotope Analysis of Archaeological Foodways and Paleoecological Interactions. PhD Dissertation, University of British Columbia (2019).

    45.
    McKechnie, I. & Moss, M. L. Meta-analysis in zooarchaeology expands perspectives on Indigenous fisheries of the Northwest Coast of North America. J. Archaeol. Sci. Rep. 8, 470–485. https://doi.org/10.1016/j.jasrep.2016.04.006 (2016).
    Article  Google Scholar 

    46.
    Efford, M. & McKechnie, I. 42nd Annual Conference of the Society of Ethnobiology May 8–11.

    47.
    Sumpter, I. D. An analysis of three shellfish assemblages from Ts’ishaa, site DfSi-16 (204T), Benson Island, Pacific Rim National Park Reserve. In Ts’ishaa: Archaeology and Ethnography of a Nuu-chah-nulth Origin Site in Barkley Sound (eds McMillan, A. D. & St. Claire, D. E.) 136–172 (Archaeology Press, Simon Fraser University, Burnaby, 2005).
    Google Scholar 

    48.
    Hay, D. E., McCarter, P. B., Kronlund, R. & Roy, C. Spawning areas of British Columbia herring: a review, geographical analysis and classification. Can. MS Rep. Fish. Aquat. Sci. 1–6, 2019 (2004).
    Google Scholar 

    49.
    St. Claire, D. E. Barkley sound tribal territories. In Between Ports Alberni and Renfrew: Notes on West Coast Peoples, Vol. 121 Mercury Series (eds Arima, E. Y. et al.) 13–202 (Canadian Ethnology Service, Canadian Museum of Civilization, Gatineau, 1991).
    Google Scholar 

    50.
    Wright, C. A., Dallimore, A., Thomson, R. E., Patterson, R. T. & Ware, D. M. Late holocene paleofish populations in Effingham Inlet, British Columbia, Canada. Palaeoecology 224, 367–384 (2005).
    Article  Google Scholar 

    51.
    Losey, R. J., Guiry, E., Nomokonova, T., Gusev, A. V. & Szpak, P. Storing fish?: a dog’s isotopic biography provides insight into Iron Age food preservation strategies in the Russian Arctic. Arch. & Anth. Sci. 12, 200. https://doi.org/10.1007/s12520-020-01166-3 (2020).
    Article  Google Scholar 

    52.
    Schalk, R. F. The structure of an anadromous fish resource. In For Theory Building in Archaeology (eds Binford, L. & Binford, S.) 207–249 (Academic Press, London, 1977).
    Google Scholar 

    53.
    Gunther, E. An analysis of the first salmon ceremony. Am. Anthropol. 28, 605–617 (1926).
    Article  Google Scholar 

    54.
    Booth, A. J., Stogdale, L. & Grigor, J. A. Salmon poisoning disease in dogs on southern Vancouver Island. Can. Vet. J. 25, 2–6 (1984).
    CAS  PubMed  PubMed Central  Google Scholar 

    55.
    Mack, C. Big Dog/Little Horse—ethnohistorical and linguistic evidence for the changing role of dogs on the Mid-and-Lower Columbia in the nineteenth century. J. Northwest Anthropol. 49, 61–70 (2015).
    Google Scholar 

    56.
    Bryan, H. M. et al. Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 139, 781–790 (2012).
    PubMed  Article  Google Scholar 

    57.
    Darimont, C. T., Reimchen, T. E. & Paquet, P. C. Foraging behaviour by gray wolves on salmon streams in coastal British Columbia. Can. J. Zool. 81, 349–353 (2003).
    Article  Google Scholar 

    58.
    Price, M. H. H. et al. Genetics of century-old fish scales reveal population patterns of decline. Conserv. Lett. 12, e12669 (2019).
    Article  Google Scholar 

    59.
    Thompson, T. Q. et al. Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations. PNAS https://doi.org/10.1073/pnas.1811559115 (2019).
    Article  PubMed  Google Scholar 

    60.
    Jewitt, J. R. A Narrative of the Adventures and Sufferings of John R. Jewitt: Only Survivor of the Ship Boston During a Captivity of Nearly Three Years Among the Indians of Nootka Sound: with an Account of the Manners, Mode of Living and Religious Opinions of the Natives (Printed by Loomis, and Richards and reprinted by Rowland Hurst, Wakefield, and Published by Longman, Hurst, Rees, Orme and Brown, London, 1816).

    61.
    McKechnie, I. Investigating the complexities of sustainable fishing at a prehistoric village on western Vancouver Island, British Columbia, Canada. J. Nat. Conserv. 15, 208–222. https://doi.org/10.1016/j.jnc.2007.05.001 (2007).
    Article  Google Scholar 

    62.
    Robinson, B. G., Franke, A. & Derocher, A. E. Stable isotope mixing models fail to estimate the diet of an avian predator. Auk 135, 60–70. https://doi.org/10.1642/AUK-17-143.1 (2018).
    Article  Google Scholar 

    63.
    West, C. F. & France, C. A. Human and canid dietary relationships: comparative stable isotope analysis from the Kodiak Archipelago, Alaska. J. Ethnobiol. 35, 519–535 (2015).
    Article  Google Scholar 

    64.
    McManus-Fry, E., Knecht, R. A., Dobney, K., Richards, M. P. & Britton, K. Dog-human dietary relationships in Yup’ik western Alaska: the stable isotope and zooarchaeological evidence from pre-contact Nunalleq. J. Archaeol. Sci. Rep. 17, 964–972 (2018).
    Google Scholar 

    65.
    Rick, T. C., Culleton, B. J., Smith, C. B., Johnson, J. R. & Kennett, D. J. Stable isotope analysis of dog, fox, and human diets at a Late Holocene Chumash village (CA-SRI-2) on Santa Rosa Island, California. J. Archaeol. Sci. 38, 1385–1393 (2011).
    Article  Google Scholar 

    66.
    Tsutaya, T., Naito, Y. I., Ishida, H. & Yoneda, M. Carbon and nitrogen isotope analyses of human and dog diet in the Okhotsk culture: perspectives from the Moyoro site, Japan. Anthropol. Sci. 122, 89–99 (2014).
    Article  Google Scholar 

    67.
    Baumann, C. et al. Dietary niche partitioning among Magdalenian canids in southwestern Germany and Switzerland. Quat. Sci. Rev. 227, 106032. https://doi.org/10.1016/j.quascirev.2019.106032 (2020).
    Article  Google Scholar 

    68.
    Feranec, R. S. & Hart, J. P. Fish and Maize: Bayesian mixing models of fourteenth- through seventeenth-century AD ancestral Wendat diets, Ontario, Canada. Sci. Rep. 9, 16658. https://doi.org/10.1038/s41598-019-53076-7 (2019).
    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar  More

  • in

    Assessing harbour porpoise carcasses potentially subjected to grey seal predation

    When assessing the ecological status and the development of populations, one important factor to consider is the mortality rate and its underlying causes15. If the status of a population is deemed unsustainable due to high mortality rates, this information can then be used to develop and implement specific management measures, for example addressing the major causes of unnatural mortality16. With regard to the potential ecological relevance of the phenomenon of grey seal predation, it is therefore also important to have reliable estimates of harbour porpoise mortalities resulting from grey seal predation as one natural cause. To allow for a standardised assessment of lesions found in suspected grey seal predation cases, this study aims to summarise the knowledge that has been gathered to date.
    The parameters described resemble the most commonly detected lesions in “definite”, “likely” and “fox” related cases of the 246 stranding records categorised as “suspicious” in terms of grey seal predation from the coasts of Schleswig–Holstein. With regard to grey seal predation, parameters 1–9 represent typical lesions, whereas the presence of parameters 10 and 11 is consistent with an interaction with a red fox.
    Similar to lesions detected in seals, lesions in porpoises most often resemble puncture lesions in the skin and blubber (parameter 1). Yet, visually most striking is the commonly detected large tissue defect with straight, cut-like wound margins with often flaps of skin and blubber remaining only partly attached to the body (parameters 2, 5, 7). Missing blubber (parameter 4) is also recorded, either as reduced blubber thickness on the flaps of skin or as fully removed parts of blubber and skin. As has been described for seals14, the lesion most often originates in the cervical area (parameter 3). A difference that has been detected between the lesions in seals and porpoises is the rate of clear parallel running bite and / or scratch marks in the skin of the animals. Whereas this is rarely detected in seals14, most porpoises show respective marks (parameter 6). One probable explanation for this dissimilarity could be the different physical and morphological properties of the two types of skin. Seal skin is very dense and elastic; tearing and rupturing the skin requires a considerable amount of force17. Porpoise skin, however, is rather susceptible to applied mechanic force and puncturing or tearing it requires comparably little force18. These different mechanical properties might also be the reason why rake marks are found in the blubber (parameter 9) more often in seals (91% of likely cases14) than in porpoises (62% of likely cases). For seals, in the majority of cases, little to no skin is missing (skin missing in 49% of likely cases14), whereas in porpoises, a considerable number of cases (81% of likely cases) have been found where skin is missing (parameter 7). Grey seals have been described to mainly target the energy rich blubber tissue of their prey11,14. For the elastic and robust seal skin, this is done by scraping off the blubber with the teeth. As porpoise skin is fragile, we suggest that the blubber, including the skin, is more often fully removed by the grey seal and swallowed whole. If true, this may also influence the net energetic gain, which is acquired by the predator. Scraping of blubber tissue from seal skin will likely yield less tissue and cost more energy than tearing off whole pieces of blubber (including skin). Thus, it may result in a lower energetic gain. However, it is still unclear if the process of catching a porpoise in comparison to younger seals might also cost a considerably larger amount of energy, negatively influencing the net gain.
    Similar to what has been described for seals, the avulsion of one or both scapulae (parameter 8) can be found and is also likely the result of the force applied when detaching the epidermis and blubber from the body of the prey14.
    For porpoises, all nine suggested parameters were found in the definite case of grey seal predation. Parameters 1–5 showed a very high (100%) and parameter 6 a high rate (95%) of occurrence in likely cases. Parameters 7–9 occurred less frequently but were still found in > 60% of all likely predation cases. These high rates of occurrence throughout all parameters suggest that wound patterns found in porpoises are less variable than the patterns found in seals14. Whether this difference is a result of the different mechanical skin properties or if other factors are responsible, is beyond the scope of this study.
    While for seals a skeletal trauma is used as an indicator of grey seal predation, for respective harbour porpoise cases, this is hardly ever (19% of likely cases) documented. In contrast, for porpoises, a skeletal trauma (parameter 10) is quite frequently detected in cases related to scavenging by foxes (46% of fox cases) where for example extremities can be manipulated19. As has been reported in seals14, the most often detected parameter in fox related cases is the ragged wound margin (parameter 11, 94% of the cases). Therefore, this can be seen as a good indicator of an interaction with a fox in porpoises. This is also supported by a definite case of fox scavenging, which was confirmed using genetic methods20. It needs to be stated though, that scavenging by birds can result in similar looking lesions, increasing the chance of misinterpretation. Scavenging by birds usually also leaves an irregular wound margin with extensive tissue loss. If parallel running lesions are present, the origin of the lesion can additionally be assessed by measuring the distances in between adjacent lesions and comparing them to published values of grey seal, fox and cetacean inter-teeth distances e.g.1. This is especially important when differentiating between for example rake marks by dolphins, which have been documented in porpoises21,22 and marks induced by grey seals. Here, it can be useful to assess the pattern of inter-teeth distances with those of dolphins expected to be consistent in length, whereas for grey seals, variable distances are expected as the result of the polydont dental morphology23. Despite a lack of available data, a differentiation between grey seal claw-induced marks and dolphin rake marks should be possible, as distances between claws of a subadult / adult grey seal male are expected to be considerably larger than for dolphin inter-teeth distances.
    Single puncture lesions, in turn, are not considered as a very good indicator despite being present in the definite and all of the likely cases. Mainly due to the susceptibility of the porpoise skin, such lesions can have many different causes (e.g. feeding by birds).
    Whether a loss of muscle tissue can be attributed to grey seal predation or is largely caused by scavengers like gulls as has been suggested for seals14, is still not entirely clear. In German as well as bordering waters, no clear pattern prevails. Carcasses with mainly intact as well as fully removed muscle tissue have been documented c.f.13. However, the reports by Stringell et al.4 suggest that not only the blubber tissue is targeted, but that there may also be some individual behavioural variation.
    The findings and the resulting parameters described here are in line with wound patterns reported in earlier publications from other areas1,6,7,13. This shows that the documented wound patterns make a reliable set of parameters when assessing harbour porpoises carcasses potentially predated by a grey seal and should be used in future assessments.
    As a complementary tool to the suggested parameters, corresponding to porpoises, we developed a decision tree with the aim of supporting a standardised and information-based decision-making process. Despite an accuracy in decision-making of 96% when using our data set, the example in Fig. 5 illustrates the limitations of such static tools when it comes to judging more complex cases. Furthermore, when comparing the suggestion given by the tree with the one made by the experts, in only 50% of unmatched cases, a rather precautionary judgement was made, bearing the risk of an overestimation of case numbers. Therefore, we recommend using the suggested tree only as an informational tool in supporting decision-making and final judgments should always be made by the responsible expert based on all available information.
    In addition to cases for which the attack of a grey seal directly led to the death of the animal, interestingly, it seems not unusual that porpoises escape this predator. Several observations have been described in the literature5,6,13,24 and nine cases were documented in German waters (Figs. 1, 2). In order to be able to verify the origin of recorded teeth marks in porpoise skin, it is crucial to record marks in detail including their pattern, location and inter-teeth distances. Using the latter, for example, interactions with dolphins can potentially be excluded. Although there has been the odd case of a severely injured seal showing comparable lesions to what is associated with grey seal predation14, such high rates of escape cases as described for porpoises have not been reported.
    Despite the co-occurrence of porpoises and grey seals in the Baltic, no case of grey seal predation on a porpoise can be confirmed by the presented results. It remains unclear whether grey seals in this area of the Baltic just don’t prey on porpoises or whether other factors like differences in behaviour (e.g. primary area of predation further offshore) are involved.
    Some of the observed behaviour of grey seals when catching a porpoise can be directly linked to the detected lesions. For example, Stringell et al.4 as well as Bouveroux et al.7 described the grey seal acting as an ambush predator and attacking the porpoise from below using its jaws to catch and retain the prey. Lesions starting in the throat area (parameter 3) combined with parallel multifocal puncture lesions (parameter 6) resemble what would be expected as the result of such an attack.
    Despite a lower rate of variability in detected wound patterns in porpoise carcasses, care should be applied when assessing lesions, as there is always the chance of other factors being involved. Therefore, if possible, a combination of data sources (necropsy results, genetic detection of predator DNA, indicators at the stranding site, eye witness reports, etc.) should be used in a systematic evaluation.
    Future research should focus on continuing thorough investigations of stranded marine mammal carcasses in order to further update and refine the suggested set of parameters. Additionally, results of current as well as retrospective analysis of stranding data should be used to support an evaluation of the ecological relevance of this behaviour. More

  • in

    Modelling the effects of CO2 on C3 and C4 grass competition during the mid-Pleistocene transition in South Africa

    1.
    Mucina, L. & Rutherford, M. C. The Vegetation of South Africa, Lesotho and Swaziland (South African National Biodiversity Institute, Pretoria, 2006).
    Google Scholar 
    2.
    van Zinderen Bakker, E. M. The evolution of late Quaternary paleoclimates of Southern Africa. Palaeoecol. Afr. 9, 160–202 (1976).
    Google Scholar 

    3.
    Cockcroft, M. J., Wilkinson, M. J. & Tyson, P. D. The application of a present-day climatic model to the late Quaternary in southern Africa. Clim. Change 10, 161–181 (1987).
    ADS  Google Scholar 

    4.
    Chase, B. M. & Meadows, M. E. Late Quaternary dynamics of southern Africa’s winter rainfall zone. Earth Sci. Rev. 84(3), 103–138 (2007).
    ADS  Google Scholar 

    5.
    Bistinas, I., Harrison, S. P., Prentice, I. C. & Pereira, J. M. C. Causal relationships vs. emergent patterns in the global controls of fire frequency. Biogeosciences 11, 5087–5101 (2014).
    ADS  Google Scholar 

    6.
    Hoetzel, S., Dupont, L., Schefuß, E., Rommerskirchen, F. & Wefer, G. The role of fire in Miocene to Pliocene C 4 grassland and ecosystem evolution. Nat. Geosci. 6(12), 1027–1030 (2013).
    ADS  CAS  Google Scholar 

    7.
    Bond, W. J., Woodward, F. I. & Midgley, G. F. The global distribution of ecosystems in a world without fire. New Phytol. 165(2), 525–538 (2005).
    CAS  PubMed  Google Scholar 

    8.
    Ripley, B. et al. Fire ecology of C3 and C4 grasses depends on evolutionary history and frequency of burning but not photosynthetic type. Ecology 96(10), 2679–2691 (2015).
    PubMed  Google Scholar 

    9.
    Pinto, H., Sharwood, R. E., Tissue, D. T. & Ghannoum, O. Photosynthesis of C3, C3–C4, and C4 grasses at glacial CO2. J. Exp. Bot. 65(13), 3669–3681 (2014).
    PubMed  PubMed Central  Google Scholar 

    10.
    Roth-Nebelsick, A. & Konrad, W. Habitat responses of fossil plant species to palaeoclimate—possible interference with CO2?. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, 277–286 (2017).
    Google Scholar 

    11.
    Ehleringer, J. R., Cerling, T. E. & Helliker, B. R. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112(3), 285–299 (1997).
    ADS  PubMed  Google Scholar 

    12.
    Edwards, E. J., Osborne, C. P., Strömberg, C. A., Smith, S. A. & C4 Grasses Consortium. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328(5978), 587–591 (2010).
    CAS  PubMed  Google Scholar 

    13.
    Hönisch, B., Hemming, N. G., Archer, D., Siddall, M. & McManus, J. F. Atmospheric carbondioxide concentration across the mid-Pleistocene transition. Science 324(5934), 1551–1554 (2009).
    ADS  PubMed  Google Scholar 

    14.
    Yan, Y. et al. Two-million-year-old snapshots of atmospheric gases from Antarctic ice. Nature 574(7780), 663–666 (2019).
    ADS  CAS  PubMed  Google Scholar 

    15.
    Faith, J. T., Rowan, J. & Du, A. Early hominins evolved within non-analog ecosystems. Proc. Natl. Acad. Sci. 116(43), 21478–21483 (2019).
    ADS  CAS  PubMed  Google Scholar 

    16.
    Sealy, J., Naidoo, N., Hare, V. J., Brunton, S. & Faith, J. T. Climate and ecology of the palaeo-Agulhas Plain from stable carbon and oxygen isotopes in bovid tooth enamel from Nelson Bay Cave, South Africa. Quat. Sci. Rev. 235, 105974 (2019).
    Google Scholar 

    17.
    Horwitz, L. K. & Chazan, M. Past and present at Wonderwerk Cave (Northern Cape Province, South Africa). Afr. Archaeol. Rev. 32(4), 595–612 (2015).
    Google Scholar 

    18.
    Ecker, M. et al. The palaeoecological context of the Oldowan-Acheulean in southern Africa. Nat. Ecol. Evol. 2(7), 1080–1086 (2018).
    PubMed  Google Scholar 

    19.
    Matmon, A. et al. New chronology for the southern Kalahari Group sediments with implications for sediment-cycle dynamics and early hominin occupation. Quat. Res. 84(1), 118–132 (2015).
    Google Scholar 

    20.
    Vainer, S., Erel, Y. & Matmon, A. Provenance and depositional environments of Quaternary sediments in the southern Kalahari Basin. Chem. Geol. 476, 352–369 (2018).
    ADS  CAS  Google Scholar 

    21.
    Prentice, I. C. et al. Modeling fire and the terrestrial carbon balance. Glob. Biogeochem. Cycles 25(3), 2–13 (2011).
    Google Scholar 

    22.
    Braconnot, P. et al. Results of PMIP2 coupled simulations of the Mid-Holocene and Last Glacial Maximum-Part 1: experiments and large-scale features. Clim. Past 3(2), 261–277 (2007).
    Google Scholar 

    23.
    Kelley, D. I. et al. A comprehensive benchmarking system for evaluating global vegetation models. Biogeosciences 10(5), 3313–3340 (2013).
    ADS  Google Scholar 

    24.
    Chazan, M. et al. Archaeology, paleoenvironment and chronology of the early middle stone age component of Wonderwerk cave in the interior of southern Africa. J. Palaeolithic Archaeol. https://doi.org/10.1007/s41982-020-00051-8 (2020).
    Article  Google Scholar 

    25.
    Lee-Thorp, J. A. & Beaumont, P. B. Vegetation and seasonality shifts during the late Quaternary deduced from 13C/12C ratios of grazers at Equus Cave, South Africa. Quat. Res. 43, 426–432 (1995).
    Google Scholar 

    26.
    Vogel, J. C. The geographical distribution of Kranz species in southern Africa. South Afr. J. Sci. 75, 209–215 (1978).
    Google Scholar 

    27.
    Zhou, H., Helliker, B. R., Huber, M., Dicks, A. & Akçay, E. C4 photosynthesis and climate through the lens of optimality. Proc. Natl. Acad. Sci. 115(47), 12057–12062 (2018).
    CAS  PubMed  Google Scholar 

    28.
    Rubin, F., Palmer, A. R. & Tyson, C. Patterns of endemism within the Karoo National Park, South Africa. Bothalia 31(1), 117–133 (2001).
    Google Scholar 

    29.
    Walker, S. J., Lukich, V. & Chazan, M. Kathu townlands: a high density earlier stone age locality in the interior of South Africa. PLoS ONE 9(7), e103436 (2014).
    ADS  PubMed  PubMed Central  Google Scholar 

    30.
    Lee-Thorp, J. A., Sponheimer, M. & Luyt, J. Tracking changing environments using stable carbon isotopes in fossil tooth enamel: an example from the South African hominin sites. J. Hum. Evol. 53(5), 595–601 (2007).
    PubMed  Google Scholar 

    31.
    Codron, D., Brink, J. S., Rossouw, L. & Clauss, M. The evolution of ecological specialization in southern African ungulates: competition- or physical environmental turnover?. Oikos 117, 344–353 (2008).
    Google Scholar 

    32.
    Plummer, T. W. et al. The environmental context of Oldowan hominin activities at Kanjera South, Kenya. In Interdisciplinary approaches to the Oldowan (eds Hovers, E. & Braun, D. R.) 149–160 (Springer, Berlin, 2009).
    Google Scholar 

    33.
    Cerling, T. E. et al. Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma. Proc. Natl. Acad. Sci. 112(37), 11467–11472 (2015).
    ADS  CAS  PubMed  Google Scholar 

    34.
    Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data. https://doi.org/10.1038/s41597-020-0453-3 (2020).
    Article  PubMed  PubMed Central  Google Scholar 

    35.
    Sitch, S. et al. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob. Change Biol. 9(2), 161–185 (2003).
    ADS  Google Scholar 

    36.
    Thonicke, K. et al. The influence of vegetation, fire spread and fire behaviour on biomass burning and trace gas emissions: results from a process-based model. Biogeosciences 7(6), 1991–2011 (2010).
    ADS  CAS  Google Scholar 

    37.
    Haxeltine, A. & Prentice, I. C. BIOME3: an equilibrium terrestrial biosphere model based on ecophysiological constraints, resource availability, and competition among plant functional types. Glob. Biogeochem. Cycles 10(4), 693–709 (1996).
    ADS  CAS  Google Scholar 

    38.
    Haxeltine, A. & Prentice, I. C. A general model for the light-use efficiency of primary production. Funct. Ecol. 10, 551–561 (1996).
    Google Scholar 

    39.
    Farquhar, G. D., Von Caemmerer, S. & Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 plants. Planta 149, 78–90 (1980).
    CAS  PubMed  PubMed Central  Google Scholar 

    40.
    Farquhar, G. D. & Von Caemmerer, S. Modelling of photosynthetic response to environmental conditions. In Physiological Plant Ecology II: Water Relations and Carbon Assimilation (eds Nobel, P. S. et al.) 549–587 (Springer, Berlin, 1982).
    Google Scholar 

    41.
    Monteith, J. L. A reinterpretation of stomatal responses to humidity. Plant Cell Environ. 18, 357–364 (1995).
    Google Scholar 

    42.
    Rothermel, R. C. A Mathematical Model for Predicting Fire Spread in Wildland Fuels (Vol. 115). Intermountain Forest and Range Experiment Station, Forest Service, US Department of Agriculture (1972).

    43.
    Sato, H., Kelley, D. I., Mayor, S. J., Cowling S. A., Calvo, M. M. & Prentice, I. C. Fire and low CO2 opened dry corridors in South America during the Last Glacial Maximum. Under Review for Nature Geosciences: NGS-2019–07–01558B (2020).

    44.
    Prentice, I. C., Harrison, S. P. & Bartlein, P. J. Global vegetation and terrestrial carbon cycle changes after the last ice age. New Phytol. 189(4), 988–998 (2011).
    CAS  PubMed  Google Scholar  More

  • in

    Deep longitudinal multiomics profiling reveals two biological seasonal patterns in California

    Cohort and data description
    In order to examine seasonal changes of human molecular data, we leveraged the power of longitudinal multiomics data from profiling of 105 individuals (55 women and 50 men) with ages ranging from 25 to 75 years old (Fig. 1a; Supplementary Table 1). This cohort was generally healthy and well characterized for glucose dysregulation using annual oral glucose tolerance tests (OGTTs), insulin resistance measuring steady-state plasma glucose (SSPG), fasting glucose and hemoglobin A1c (HbA1c; an indicator of the average level of blood glucose over the past 100 days)19 as well as quarterly sample collections with measurements of transcriptomes (from peripheral blood mononuclear cells), proteome and metabolome from plasma, targeted cytokine and growth factor assays using serum. Nasal and gut microbiomes were analyzed using 16S rRNA sequencing providing information at the genus level and host exome sequencing was performed once from PBMCs (Fig. 1b). Moreover, 51 clinical laboratory tests were acquired on each visit and they were aligned to the meteorological data (e.g. air temperature), pollen counts (e.g. mold spores, grass pollens, tree pollens, weed pollens) and airborne fungi from the San Francisco bay area. In total, there were 902 visits (average across different types of omes‘) from which samples were drawn over up to 4 years (see “Methods”). The sample collections were generally evenly distributed throughout the year (Fig. 1b). Nearly all individuals lived in the San Francisco Bay Area with the exception of three individuals who lived in Southern California and frequented the Bay area (Supplementary Data 1). Participants in our study were well characterized for steady-state plasma glucose (SSPG) using the modified insulin suppression test20, in which 31 participants were insulin sensitive (SSPG  0.05, Supplementary Table 5, Supplementary Fig. 10). In our analysis we used subject ID as a random effect to account for different numbers of samples per subject. On the other hand, physical activity measured in total metabolic equivalent of task (MET) is significantly different between the IR and the IS groups in February, May, June, and August (P-value = 0.01787, Supplementary Fig. 11). However, a post-hoc analysis of all the omics features that were identified to be significantly different between the IR and the IS groups, are not associated with the physical activity. More

  • in

    Differential side-effects of Bacillus thuringiensis bioinsecticide on non-target Drosophila flies

    1.
    United Nations, Department of Economic and Social Affairs, Population Division. World Population Prospects 2019—Data Booklet (ST/ESA/ SER.A/377), (2019). https://population.un.org/wpp/Publications/Files/WPP2019_DataBooklet.pdf
    2.
    Pimentel, D. & Burgess, M. Environmental and economic costs of the application of pesticides primarily in the United States. In Integrated Pest Management: Innovation-Development Process (eds Peshin, R. & Dhawan, A. K.) 47–71 (Springer, Dordrecht, 2014). https://doi.org/10.1007/978-1-4020-8992-3_4
    Google Scholar 

    3.
    Devine, G. J. & Furlong, M. J. Insecticide use: Contexts and ecological consequences. Agric. Hum. Values 24(3), 281–306. https://doi.org/10.1007/s10460-007-9067-z (2007).
    Article  Google Scholar 

    4.
    Sanchis, V. & Bourguet, D. Bacillus thuringiensis: Applications in agriculture and insect resistance management. A review. Agron. Sustain. Dev. 28(1), 11–20. https://doi.org/10.1051/agro:2007054 (2008).
    Article  Google Scholar 

    5.
    WHO report. WHO specifications and evaluations for public health pesticides: Bacillus thuringiensis subspecies israelensis strain AM65-52. (World Health Organization, Geneva, 2007).

    6.
    Rizzati, V., Briand, O., Guillou, H. & Gamet-Payrastre, L. Effects of pesticide mixtures in human and animal models: An update of the recent literature. Chem. Biol. Interact. 254, 231–246. https://doi.org/10.1016/j.cbi.2016.06.003 (2016).
    Article  PubMed  CAS  Google Scholar 

    7.
    Lacey, L. A. et al. Insect pathogens as biological control agents: Back to the future. J. Invertebr. Pathol. 132, 1–41. https://doi.org/10.1016/j.jip.2015.07.009 (2015).
    Article  PubMed  CAS  Google Scholar 

    8.
    Adang, M. J., Crickmore, N. & Jurat-Fuentes, J. L. Diversity of Bacillus thuringiensis Crystal Toxins and Mechanism of Action. Adv. Insect Physiol. 47, 39–87. https://doi.org/10.1016/B978-0-12-800197-4.00002-6 (2014).
    Article  Google Scholar 

    9.
    Crickmore, N. Bacillus thuringiensis toxin classification. In Bacillus thuringiensis and Lysinibacillus sphaericus. (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 41-52, (Spinger, Cham, 2017).

    10.
    WHO report. Guideline specification for bacterial larvicides for public health use. WHO document WHO/CDS/CPC/WHOPES/99.2 (World Health Organization, Geneva, 1999).

    11.
    Bravo, A., Pacheco, S., Gomez, I., Garcia-Gomez B., Onofre, J., Soberon, M. Insecticidal Proteins from Bacillus thuringiensis and their Mechanism of Action. In Bacillus thuringiensis and Lysinibacillus sphaericus (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 53–66, (Spinger, Cham, 2017).

    12.
    Palma, L., Muñoz, D., Berry, C., Murillo, J. & Caballero, P. Bacillus thuringiensis toxins: An overview of their biocidal activity. Toxins 6(12), 3296–3325. https://doi.org/10.3390/toxins6123296 (2014).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    13.
    Ben-Dov, E. et al. Extended screening by PCR for seven cry-group genes from field-collected strains of Bacillus thuringiensis. Appl. Environ. Microb. 63(12), 4883–4890. https://doi.org/10.1128/aem.63.12.4883-4890.1997 (1997).
    CAS  Google Scholar 

    14.
    Berry, C. et al. Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl. Environ. Microbiol. 68(10), 5082–5095. https://doi.org/10.1128/aem.68.10.5082-5095.2002 (2002).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    15.
    Bravo, A., Gill, S. S. & Soberon, M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49, 423–435. https://doi.org/10.1016/j.toxicon.2006.11.022 (2007).
    Article  PubMed  CAS  Google Scholar 

    16.
    Wei, J. et al. Activation of Bt protoxin Cry1Ac in resistant and susceptible cotton bollworm. PLoS ONE 11(6), e0156560. https://doi.org/10.1371/journal.pone.0156560 (2016).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    17.
    Bravo, A., Likitvivatanavong, S., Gill, S. S. & Soberon, M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41(7), 423–431. https://doi.org/10.1016/j.ibmb.2011.02.006 (2011).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    18.
    Caccia, S. et al. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proc. Natl. Acad. Sci. USA 113(34), 9486–9491. https://doi.org/10.1073/pnas.1521741113 (2016).
    Article  PubMed  CAS  Google Scholar 

    19.
    Glare, T.R., O’Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety. ISBN: 9780471496304, 350, (Wiley, New York, 2000).

    20.
    Rubio-Infante, N. & Moreno-Fierros, L. An overview of the safety and biological effects of Bacillus thuringiensis Cry toxins in mammals. J. Appl. Toxicol. 36, 630–648. https://doi.org/10.1002/jat.3252 (2016).
    Article  PubMed  CAS  Google Scholar 

    21.
    EFSA Panel on Biological Hazards (BIOHAZ). Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs. EFSA J. https://doi.org/10.2903/j.efsa.2016.4524 (2016).
    Article  Google Scholar 

    22.
    Amichot, M., Curty, C., Benguettat-Magliano, O., Gallet, A. & Wajnberg, E. Side effects of Bacillus thuringiensis var. kurstaki on the hymenopterous parasitic wasp Trichogramma chilonis. Environ. Sci. Pollut. Res. Int. 23, 3097–3103. https://doi.org/10.1007/s11356-015-5830-7 (2016).
    Article  PubMed  CAS  Google Scholar 

    23.
    Renzi, M. T. et al. Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined. Ecotoxicol. Environ. Saf. 127, 205–213. https://doi.org/10.1016/j.ecoenv.2016.01.028 (2016).
    Article  PubMed  CAS  Google Scholar 

    24.
    Caquet, T., Roucaute, M., Le Goff, P. & Lagadic, L. Effects of repeated field applications of two formulations of Bacillus thuringiensis var. israelensis on non-target saltmarsh invertebrates in Atlantic coastal wetlands. Ecotoxicol. Environ. Saf. 74, 1122–1130. https://doi.org/10.1016/j.ecoenv.2011.04.028 (2011).
    Article  PubMed  CAS  Google Scholar 

    25.
    Duguma, D. et al. Microbial communities and nutrient dynamics in experimental microcosms are altered after the application of a high dose of Bti. J. Appl. Ecol. 52, 763–773. https://doi.org/10.1111/1365-2664.12422 (2015).
    Article  CAS  Google Scholar 

    26.
    Venter, H. J. & Bøhn, T. Interactions between Bt crops and aquatic ecosystems: A review. Environ. Toxicol. Chem. 35(12), 2891–2902. https://doi.org/10.1002/etc.3583 (2016).
    Article  PubMed  CAS  Google Scholar 

    27.
    van Frankenhuyzen, K. Specificity and cross-order activity of Bacillus thuringiensis pesticidal proteins. In Bacillus thuringiensis and Lysinibacillus sphaericus (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 127–172, (Springer, Cham, 2017).

    28.
    Bizzarri, M. F. & Bishop, A. H. The ecology of Bacillus thuringiensis on the phylloplane: Colonization from soil, plasmid transfer, and interaction with larvae of Pieris brassicae. Microb. Ecol. 56(1), 133–139. https://doi.org/10.1007/s00248-007-9331-1 (2008).
    Article  PubMed  CAS  Google Scholar 

    29.
    Raymond, B., Wyres, K. L., Sheppard, S. K., Ellis, R. J. & Bonsall, M. B. Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathog. 6(5), e1000905. https://doi.org/10.1371/journal.ppat.1000905 (2010).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    30.
    Hendriksen, N. B. & Hansen, B. M. Long-term survival and germination of Bacillus thuringiensis var. kurstaki in a field trial. Can. J. Microbiol. 48(3), 256–261. https://doi.org/10.1139/w02-009 (2002).
    Article  PubMed  CAS  Google Scholar 

    31.
    Hung, T. P. et al. Persistence of detectable insecticidal proteins from Bacillus thuringiensis (Cry) and toxicity after adsorption on contrasting soils. Environ. Pollut. 208, 318–325. https://doi.org/10.1016/j.envpol.2015.09.046 (2016).
    Article  PubMed  CAS  Google Scholar 

    32.
    Hung, T. P. et al. Fate of insecticidal Bacillus thuringiensis Cry protein in soil: Differences between purified toxin and biopesticide formulation. Pest Manag. Sci. 72, 2247–2253. https://doi.org/10.1002/ps.4262 (2016).
    Article  PubMed  CAS  Google Scholar 

    33.
    Enger, K. S. et al. Evaluating the long-term persistence of Bacillus spores on common surfaces. Microb. Biotechnol. 11(6), 1048–1059. https://doi.org/10.1111/1751-7915.13267 (2018).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    34.
    Couch, T.L. Industrial fermentation and formulation of entomopathogenic bacteria. In Entomopathogenic Bacteria: From Laboratory to Field Application (eds Charles, J.-F. et al.) ISBN 978-90-481-5542-2, 297–316.43, (Springer, Dordrecht, 2000).

    35.
    Brar, S. K., Verma, M., Tyagi, R. D. & Valéro, J. R. Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides. Process Biochem. 41(2), 323–342. https://doi.org/10.1016/j.procbio.2005.07.015 (2006).
    Article  CAS  Google Scholar 

    36.
    Setlow, P. Spore resistance properties. Microbiol. Spectr. 2(5), TBS-0003-2012. https://doi.org/10.1128/microbiolspec.TBS-0003-2012 (2014).
    Article  CAS  Google Scholar 

    37.
    European Food Safety Authority. Conclusion on the peer review of the pesticide risk assessment of the active substance Bacillus thuringiensis subsp. Kurstaki (strains ABTS 351, PB 54, SA 11, SA 12, EG 2348). EFSA J. 10(2), 2540. https://doi.org/10.2903/j.efsa.2012.2540 (2012).
    Article  CAS  Google Scholar 

    38.
    Bächli, G. TaxoDros: The database on Taxonomy of Drosophilidae: Database 2020/1.https://www.taxodros.uzh.ch. (1999–2020).

    39.
    Tennessen, J. M. & Thummel, C. S. Coordinating growth and maturation—Insights from Drosophila. Curr. Biol. 21(18), R750–R757. https://doi.org/10.1016/j.cub.2011.06.033 (2011).
    Article  PubMed  PubMed Central  CAS  Google Scholar 

    40.
    Benz, G. & Perron, J. M. The toxic action of Bacillus thuringiensis “exotoxin” on Drosophila reared in yeast-containing and yeast-free media. Experientia 23(10), 871–872 (1967).
    PubMed  CAS  Google Scholar 

    41.
    Saadoun, I., Al-Moman, F., Obeidat, M., Meqdam, M. & Elbetieha, A. Assessment of toxic potential of local Jordanian Bacillus thuringiensis strains on Drosophila melanogaster and Culex sp. (Diptera). J. Appl. Microbiol. 90, 866–872. https://doi.org/10.1046/j.1365-2672.2001.01315.x (2001).
    Article  PubMed  CAS  Google Scholar 

    42.
    Khyami-Horani, H. Toxicity of Bacillus thuringiensis and B. sphaericus to laboratory populations of Drosophila melanogaster (Diptera: Drosophilidae). J. Basic Microbiol. 42(2), 105–110. https://doi.org/10.1002/1521-4028(200205)42:23.0.CO;2-S (2002). 
    Article  PubMed  Google Scholar 

    43.
    Obeidat, M. Toxicity of local Bacillus thuringiensis isolates against Drosophila melanogaster. WJAS 4(2), 161–167 (2008).
    Google Scholar 

    44.
    Obeidat, M., Khymani-Horani, H. & Al-Momani, F. Toxicity of Bacillus thuringiensis β-exotoxins and δ-endotoxins to Drosophila melanogaster, Ephestia kuhniella and human erythrocytes. Afr. J. Biotechnol. 11(46), 10504–10512 (2012).
    Google Scholar 

    45.
    Cossentine, J., Robertson, M. & Xu, D. Biological activity of Bacillus thuringiensis in Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol. 109(3), 1–8. https://doi.org/10.1093/jee/tow062 (2016).
    Article  CAS  Google Scholar 

    46.
    Biganski, S., Jehle, J. A. & Kleepies, R. G. Bacillus thuringiensis serovar israelensis has no effect on Drosophila suzukii Matsumura. J. Appl. Entomol. 142, 33–36. https://doi.org/10.1111/jen.12415 (2017).
    Google Scholar 

    47.
    Haller, S., Romeis, J. X. R. & Meissle, M. Effects of purified or plant-produced Cry proteins on Drosophila melanogaster (Diptera: Drosophilidae) larvae. Sci. Rep. 7(1), 11172. https://doi.org/10.1038/s41598-017-10801-4 (2017).
    ADS  Article  PubMed  PubMed Central  CAS  Google Scholar 

    48.
    Benado, M. & Brncic, D. An eight-year phenological study of a local drosophilid community in Central Chile. J. Zool. Syst. Evol. Res. 32, 51–63. https://doi.org/10.1111/j.1439-0469.1994.tb00470.x (1994).
    Article  Google Scholar 

    49.
    Nunney, L. The colonization of oranges by the cosmopolitan Drosophila. Oecologia 108, 552–561. https://www.jstor.org/stable/4221451 (1996).
    ADS  PubMed  Google Scholar 

    50.
    Mitsui, H. & Kimura, M. T. Coexistence of drosophilid flies: Aggregation, patch size diversity and parasitism. Ecol. Res. 15, 93–100.  https://doi.org/10.1046/j.1440-1703.2000.00328.x (2000).
    Google Scholar 

    51.
    Withers, P. & Allemand, R. Les drosophiles de la région Rhône-Alpes (Diptera, Drosophilidae). Bull. Soc. Entomol. Fr. 117(4), 473–482. https://www.persee.fr/doc/bsef_0037-928x_2012_num_117_4_3076 (2012).
    Google Scholar 

    52.
    Stevens, T., Song, S., Bruning, J. B., Choo, A. & Baxter, S. W. Expressing a moth abcc2 gene in transgenic Drosophila causes susceptibility to Bt Cry1Ac without requiring a cadherin-like protein receptor. Insect Biochem. Mol. Biol. 80, 61–70. https://doi.org/10.1016/j.ibmb.2016.11.008 (2017).
    Article  PubMed  CAS  Google Scholar 

    53.
    George, Z., Crickmore, N. Bacillus thuringiensis applications in agriculture. In Bacillus thuringiensis Biotechnology (ed Sansinenea, E.) 392, (Springer, Dordrecht, 2012).

    54.
    Nepoux, V., Haag, C. R. & Kawecki, T. J. Effects of inbreeding on aversive learning in Drosophila. J. Evol. Biol. 23, 2333–2345. https://doi.org/10.1111/j.1420-9101.2010.02094.x (2010).
    Article  PubMed  CAS  Google Scholar 

    55.
    Vantaux, A., Ouattarra, I., Lefèvre, T. & Dabiré, K. R. Effects of larvicidal and larval nutritional stresses on Anopheles gambiae development, survival and competence for Plasmodium falciparum. Parasite. Vector. 9, 226. https://doi.org/10.1186/s13071-016-1514-5 (2016).
    Article  CAS  Google Scholar 

    56.
    Moret, Y. & Schmid-Hempel, P. Survival for immunity: The price of immune system activation for bumblebee workers. Science 290(5494), 1166–1168. https://doi.org/10.1126/science.290.5494.1166 (2000).
    ADS  Article  PubMed  CAS  Google Scholar 

    57.
    Kutzer, M. A. & Armitage, S. A. O. The effect of diet and time after bacterial infection on fecundity, resistance, and tolerance in Drosophila melanogaster. Ecol. Evol. 6(13), 4229–4242. https://doi.org/10.1002/ece3.2185 (2016).
    Article  PubMed  PubMed Central  Google Scholar 

    58.
    Andersen, L. H., Kristensen, T. N., Loeschcke, V., Toft, S. & Mayntz, D. Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosophila melanogaster. J. Insect Physiol. 56, 336–340. https://doi.org/10.1016/j.jinsphys.2009.11.006 (2010).
    Article  PubMed  CAS  Google Scholar 

    59.
    Rion, S. & Kawecki, T. J. Evolutionary biology of starvation resistance: What we have learned from Drosophila. J. Evol. Biol. 20(5), 1655–1664. https://doi.org/10.1111/j.1420-9101.2007.01405.x (2007).
    Article  PubMed  CAS  Google Scholar 

    60.
    Burger, J. M. S., Buechel, S. D. & Kawecki, T. J. Dietary restriction affects lifespan but not cognitive aging in Drosophila melanogaster. Aging Cell 9, 327–335. https://doi.org/10.1111/j.1474-9726.2010.00560.x (2010).
    Article  PubMed  CAS  Google Scholar 

    61.
    Khazaeli, A. A. & Curtsinger, J. W. Genetic analysis of extended lifespan in Drosophila melanogaster III. On the relationship between artificially selected and wild stocks. Genetica 109, 245–253. https://doi.org/10.1023/a:1017569318401 (2000).
    Article  PubMed  CAS  Google Scholar 

    62.
    Atkinson, W. & Shorrocks, B. Breeding site specificity in the domestic species of Drosophila. Oecologia 29(3), 223–232. https://www.jstor.org/stable/4215461 (1977).
    ADS  PubMed  CAS  Google Scholar 

    63.
    Walsh, D. B. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integr. Pest Manag. https://doi.org/10.1603/IPM10010 (2011).
    Article  Google Scholar 

    64.
    Delbac, L. et al. Drosophila suzukii est-elle une menace pour la vigne?. Phytoma 679, 16–21 (2014).
    Google Scholar 

    65.
    Poyet, M. et al. Invasive host for invasive pest: When the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotine) in Europe. Agric. For. Entomol. 16(3), 251–259. https://doi.org/10.1111/afe.12052 (2014).
    Article  Google Scholar 

    66.
    Poulin, B., Lefebvre, G. & Paz, L. Red flag for green spray: Adverse trophic effects of Bti on breeding birds. J. Appl. Ecol. 47, 884–889. https://doi.org/10.1111/j.1365-2664.2010.01821.x (2010).
    Article  Google Scholar 

    67.
    Zeigler, D.R. Bacillus genetic stock center catalog of strains, 7th edition. Part 2: Bacillus thuringiensis and Bacillus cereus. http://www.bgsc.org/_catalogs/Catpart2.pdf (1999).

    68.
    Gonzales, J. M. Jr., Brown, B. J. & Carlton, B. C. Transfer of Bacillus thuringiensis plasmids coding for δ-endotoxin among strains of B. thuringiensis and B. cereus. Proc. Natl Acad. Sci. USA 79, 6951–6955. https://doi.org/10.1073/pnas.79.22.6951 (1982).
    ADS  Article  Google Scholar 

    69.
    Santos, M., Borash, D. J., Joshi, A., Bounlutay, N. & Mueller, L. D. Density-dependent natural selection in Drosophila: Evolution of growth rate and body size. Evolution 51(2), 420–432. https://doi.org/10.2307/2411114 (1997).
    Article  PubMed  Google Scholar 

    70.
    Bradberry, S. M., Proudfoot, A. T. & Vale, J. A. Glyphosate poisoning. Toxicol. Rev. 23(3), 159–167. https://doi.org/10.2165/00139709-200423030-00003 (2004).
    Article  PubMed  CAS  Google Scholar 

    71.
    R Development Core Team. R: A language and environment for statistical computing. ISBN 3-900051-07-0 https://www.R-project.org (R Foundation for Statistical Computing, Vienna, 2008).

    72.
    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).
    Google Scholar 

    73.
    Kosmidis I. brglm: Bias Reduction in Binary-Response Generalized Linear Models. R package version 0.6.1, https://www.ucl.ac.uk/~ucakiko/software.html, (2017).

    74.
    Horton, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometrical J. 50(3), 346–363. https://doi.org/10.1002/bimj.200810425 (2008).
    MathSciNet  Article  Google Scholar 

    75.
    Therneau, T.M., Grambsch, P.M. Modeling Survival Data: Extending The Cox Model. ISBN 0-387-98784-3 (Springer, New York, 2000).

    76.
    Therneau, T.M. coxme: Mixed Effects Cox Models. R package version 2.2-5. https://CRAN.R-project.org/package=coxme (2015). More

  • in

    Utilizing conductivity of seawater for bioelectric measurement of fish

    For sustainable use of marine-animal resources, preservation of endangered species, and conservation of ecosystems, it is very important to understand the biology of individual marine animal. From the viewpoints of physiology, ethology, and environmentology, marine animals have been studied by bioelectric measurement1,2,3,4, bio-logging5,6,7,8,9, and DNA (genome) analysis10,11,12,13,14,15, respectively. Recent technological innovations helped studies on bio-logging and DNA analysis advance rapidly, but advancement of bioelectric-measurement technology, which has existed for a long time, lags behind those of bio-logging and DNA analysis.
    Now, aiming to obtain good harvests, the aquaculture industry requires bioelectric measurements to grasp the health condition of marine animals from pathophysiological viewpoints. Moreover, the electrocardiogram (ECG), which is a kind of bioelectric measurement, carries high expectations because it can evaluate psychological stress of marine animals just as it can evaluate that of humans16,17,18,19. Moreover, ECG can be used in fish ethological- and physiological studies2,4, so innovating techniques and devices for ECG measurement will contribute to developing these studies.
    In regards to bioelectric measurement targeting marine animals, to prevent electric short-circuiting between the pair of bioelectrodes via seawater (which is conductive), one or multiple pairs of bioelectrodes are embedded inside the living body by incision surgery20,21, which can impose a heavy workload on inexperienced experimenters. Moreover, the animal can often become agitated without anesthesia and consume much physical energy when the electrodes are implanted into its body. To reduce these burdens, we propose a novel method of measuring bioelectric signals—which utilizes the conductivity of seawater surrounding the animal—by using only one bioelectrode attached at each measurement point (in contrast to the conventional method, which requires a pair of bioelectrodes). To the best of our knowledge, a similar method has not been reported.
    In this paper, the proposed method of bioelectric measurement for marine animals under the seawater is first overviewed. Next, the bioelectric measurement system for the chosen experimental subjects, namely, fish, is described, and the availability of the proposed method is verified. Then, the experimental procedures and results of bioelectric measurements are presented. Finally, possible applications of the proposed method are discussed. More

  • in

    Protists as catalyzers of microbial litter breakdown and carbon cycling at different temperature regimes

    1.
    Singh BK, Bardgett RD, Smith P, Reay DS. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol. 2010;8:779–90.
    CAS  Article  Google Scholar 
    2.
    Schlesinger WH, Andrews JA. Soil respiration and the global carbon cycle. Biogeochemistry. 2000;48:7–20.
    CAS  Article  Google Scholar 

    3.
    Kallenbach CM, Frey SD, Grandy AS. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun. 2016;7:13630.
    CAS  Article  Google Scholar 

    4.
    Six J, Frey SD, Thiet RK, Batten KM. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J. 2006;70:555–69.
    CAS  Article  Google Scholar 

    5.
    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.
    CAS  Article  Google Scholar 

    6.
    Zhou J, Xue K, Xie J, Deng Y, Wu L, Cheng X, et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat Clim Change. 2012;2:106–10.
    CAS  Article  Google Scholar 

    7.
    Aerts R. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos. 1997;79:439–49.
    Article  Google Scholar 

    8.
    Bradford MA, Veen GFC, Bonis A, Bradford EM, Classen AT, Cornelissen JHC, et al. A test of the hierarchical model of litter decomposition. Nat Ecol Evol. 2017;1:1836–45.
    Article  Google Scholar 

    9.
    Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.
    CAS  Article  Google Scholar 

    10.
    Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, et al. Soil protists: a fertile frontier in soil biology research. FEMS Microbiol Rev. 2018;42:293–323.
    CAS  Article  Google Scholar 

    11.
    Oliverio AM, Geisen S, Delgado-Baquerizo M, Maestre FT, Turner BL, Fierer N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv. 2020;6:eaax8787.
    Article  Google Scholar 

    12.
    Rose JM, Vora NM, Countway PD, Gast RJ, Caron DA. Effects of temperature on growth rate and gross growth efficiency of an Antarctic bacterivorous protist. ISME J. 2009;3:252–60.
    CAS  Article  Google Scholar 

    13.
    Schulz-Bohm K, Geisen S, Wubs ERJ, Song C, de Boer W, Garbeva P. The prey’s scent—volatile organic compound mediated interactions between soil bacteria and their protist predators. ISME J. 2017;11:817–20.
    CAS  Article  Google Scholar 

    14.
    Kuikman PJ, Jansen AG, van Veen JA, Zehnder AJB. Protozoan predation and the turnover of soil organic carbon and nitrogen in the presence of plants. Biol Fertil Soils. 1990;10:22–28.
    CAS  Article  Google Scholar 

    15.
    Crowther TW, Boddy L, Hefin Jones T. Functional and ecological consequences of saprotrophic fungus–grazer interactions. ISME J. 2012;6:1992–2001.
    CAS  Article  Google Scholar 

    16.
    Bradford MA, Tordoff GM, Eggers T, Jones TH, Newington JE. Microbiota, fauna, and mesh size interactions in litter decomposition. Oikos. 2002;99:317–23.
    Article  Google Scholar 

    17.
    Jousset A, Rochat L, Pechy-Tarr M, Keel C, Scheu S, Bonkowski M. Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME J. 2009;3:666–74.
    CAS  Article  Google Scholar 

    18.
    Crowther TW, Thomas SM, Maynard DS, Baldrian P, Covey K, Frey SD, et al. Biotic interactions mediate soil microbial feedbacks to climate change. Proc Natl Acad Sci. 2015;112:7033.
    CAS  Article  Google Scholar 

    19.
    Serna-Chavez HM, Fierer N, van Bodegom PM. Global drivers and patterns of microbial abundance in soil. Glob Ecol Biogeogr. 2013;22:1162–72.
    Article  Google Scholar 

    20.
    Scharlemann JPW, Tanner EVJ, Hiederer R, Kapos V. Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag. 2014;5:81–91.
    CAS  Article  Google Scholar  More