More stories

  • in

    Experimental warming differentially affects vegetative and reproductive phenology of tundra plants

    1.Pepin, N. et al. Elevation-dependent warming in mountain regions of the world. Nat. Clim. Chang. 5, 424–430 (2015).ADS 

    Google Scholar 
    2.Cohen, J. et al. Recent Arctic amplification and extreme mid-latitude weather. Nat. Geosci. 7, 627–637 (2014).ADS 
    CAS 

    Google Scholar 
    3.Overland, J. E., Wang, M., Walsh, J. E. & Stroeve, J. C. Future Arctic climate changes: adaptation and mitigation time scales. Earth’s Future 2, 68–74 (2014).ADS 

    Google Scholar 
    4.Oberbauer, S. F. et al. Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment. Philos. Trans. R. Soc. B Biol. Sci. 368, 1624 (2013).5.Prevéy, J. S. et al. Warming shortens flowering seasons of tundra plant communities. Nat. Ecol. Evol. 3, 45–52 (2019).PubMed 

    Google Scholar 
    6.Jabis, M. D., Winkler, D. E. & Kueppers, L. M. Warming acts through earlier snowmelt to advance but not extend alpine community flowering. Ecology https://doi.org/10.1002/ecy.3108 (2020).7.Beard, K. H., Kelsey, K. C., Leffler, A. J. & Welker, J. M. The missing angle: ecosystem consequences of phenological mismatch. Trends Ecol. Evol. 34, 885–888 (2019).PubMed 

    Google Scholar 
    8.Gallinat, A. S., Primack, R. B. & Wagner, D. L. Autumn, the neglected season in climate change research. Trends Ecol. Evol. 30, 169–176 (2015).PubMed 

    Google Scholar 
    9.Semenchuk, P. R. et al. High Arctic plant phenology is determined by snowmelt patterns but duration of phenological periods is fixed: an example of periodicity. Environ. Res. Lett. 11, 125006 (2016).10.Keenan, T. F. & Richardson, A. D. The timing of autumn senescence is affected by the timing of spring phenology: Implications for predictive models. Glob. Chang. Biol. 21, 2634–2641 (2015).ADS 
    PubMed 

    Google Scholar 
    11.Diepstraten, R. A. E., Jessen, T. D., Fauvelle, C. M. D. & Musiani, M. M. Does climate change and plant phenology research neglect the Arctic tundra? Ecosphere 9, e02362 (2018).12.Savage, J. A. A temporal shift in resource allocation facilitates flowering before leaf out and spring vessel maturation in precocious species. Am. J. Bot. 106, 113–122 (2019).PubMed 

    Google Scholar 
    13.Neuner, G. Frost resistance in alpine woody plants. Front. Plant Sci. 5, 654 (2014).14.Kuprian, E., Briceño, V. F., Wagner, J. & Neuner, G. Ice barriers promote supercooling and prevent frost injury in reproductive buds, flowers and fruits of alpine dwarf shrubs throughout the summer. Environ. Exp. Bot. 106, 4–12 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    15.Vitasse, Y., Lenz, A. & Körner, C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Front. Plant Sci. 5, 1–12 (2014).
    Google Scholar 
    16.Maron, J. L., Agrawal, A. A. & Schemske, D. W. Plant–herbivore coevolution and plant speciation. Ecology 100, 1–11 (2019).
    Google Scholar 
    17.Rafferty, N. E. & Ives, A. R. Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecol. Lett. 14, 69–74 (2011).PubMed 

    Google Scholar 
    18.Fitter, A. H. & Fitter, R. S. R. Rapid changes in flowering time in British plants. Science 296, 1689–1691 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    19.Post, E. Time in Ecology: A Theoretical Framework (Princeton University Press, 2019).20.Kharouba, H. M., Vellend, M., Sarfraz, R. M. & Myers, J. H. The effects of experimental warming on the timing of a plant-insect herbivore interaction. J. Anim. Ecol. 84, 785–796 (2015).PubMed 

    Google Scholar 
    21.Zohner, C. M., Mo, L. & Renner, S. S. Global warming reduces leaf-out and flowering synchrony among individuals. Elife 7, 1–15 (2018).
    Google Scholar 
    22.Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim. Change 94, 105–121 (2009).ADS 

    Google Scholar 
    23.Bjorkman, A. D., Elmendorf, S. C., Beamish, A. L., Vellend, M. & Henry, G. H. R. Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob. Chang. Biol. 21, 4651–4661 (2015).ADS 
    PubMed 

    Google Scholar 
    24.Assmann, J. J. et al. Local snow melt and temperature—but not regional sea ice—explain variation in spring phenology in coastal Arctic tundra. Glob. Chang. Biol. 25, 2258–2274 (2019).ADS 
    PubMed 

    Google Scholar 
    25.Cooper, E. J., Dullinger, S. & Semenchuk, P. Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. Plant Sci. 180, 157–167 (2011).CAS 
    PubMed 

    Google Scholar 
    26.Kelsey, K. C. et al. Winter snow and spring temperature have differential effects on vegetation phenology and productivity across Arctic plant communities. Glob. Chang. Biol. 1–15 https://doi.org/10.1111/gcb.15505 (2020).27.Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Chang. Biol. 12, 1969–1976 (2006).ADS 

    Google Scholar 
    28.Panchen, Z. A. & Gorelick, R. Prediction of Arctic plant phenological sensitivity to climate change from historical records. Ecol. Evol. 7, 1325–1338 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    29.Livensperger, C. et al. Earlier snowmelt and warming lead to earlier but not necessarily more plant growth. AoB Plants 8, 1–15 (2016).
    Google Scholar 
    30.Livensperger, C. et al. Experimentally warmer and drier conditions in an Arctic plant community reveal microclimatic controls on senescence. Ecosphere 10, e02677 (2019).31.Piao, S. et al. Plant phenology and global climate change: current progresses and challenges. Glob. Chang. Biol. 1922–1940 https://doi.org/10.1111/gcb.14619 (2019).32.Panchen, Z. A. et al. Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes. Ann. Bot. 865–873 https://doi.org/10.1093/aob/mcv015 (2015).33.Wu, C. et al. Contrasting responses of autumn-leaf senescence to daytime and night-time warming. Nat. Clim. Chang. 8, 1092–1096 (2018).ADS 
    CAS 

    Google Scholar 
    34.Zhu, W. et al. Extension of the growing season due to delayed autumn over mid and high latitudes in North America during 1982–2006. Glob. Ecol. Biogeogr. 21, 260–271 (2012).
    Google Scholar 
    35.Liu, Q. et al. Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob. Chang. Biol. 22, 3702–3711 (2016).ADS 
    PubMed 

    Google Scholar 
    36.Richardson, A. D. et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric. Meteorol. 169, 156–173 (2013).
    Google Scholar 
    37.Marchand, F. L. et al. Climate warming postpones senescence in High Arctic Tundra. Arct. Antarct. Alp. Res. 36, 390–394 (2004).
    Google Scholar 
    38.Steltzer, H. & Post, E. Seasons and life cycles. Science 324, 886–887 (2009).PubMed 

    Google Scholar 
    39.Jiang, L. L. et al. Relatively stable response of fruiting stage to warming and cooling relative to other phenological events. Ecology 97, 1961–1969 (2016).CAS 
    PubMed 

    Google Scholar 
    40.Kharouba, H. M. et al. Global shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl Acad. Sci. USA 115, 5211–5216 (2018).CAS 
    PubMed 

    Google Scholar 
    41.Piao, S., Friedlingstein, P., Ciais, P., Viovy, N. & Demarty, J. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob. Biogeochem. Cycles 21, 1–11 (2007).
    Google Scholar 
    42.Wookey, P. A. et al. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob. Chang. Biol. 15, 1153–1172 (2009).ADS 

    Google Scholar 
    43.Arft, A. M. et al. Responses of Tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol. Monogr. 69, 491–511 (1999).
    Google Scholar 
    44.Buttler, A. et al. Experimental warming interacts with soil moisture to discriminate plant responses in an ombrotrophic peatland. J. Veg. Sci. 26, 964–974 (2015).
    Google Scholar 
    45.Healy, N. C., Oberbauer, S. F. & Hollister, R. D. Examination of surface temperature modification by open-top chambers along moisture and latitudinal gradients in Arctic Alaska using thermal infrared photography. Remote Sens. 1–19 https://doi.org/10.3390/rs8010054 (2016).46.Elmendorf, S. C. et al. Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol. Lett. 15, 164–175 (2012).PubMed 

    Google Scholar 
    47.Post, E., Steinman, B. A. & Mann, M. E. Acceleration of phenological advance and warming with latitude over the past century. Sci. Rep. 1–8 https://doi.org/10.1038/s41598-018-22258-0 (2018).48.Iler, A. M., Høye, T. T., Inouye, D. W. & Schmidt, N. M. Nonlinear flowering responses to climate: Are species approaching their limits of phenological change? Philos. Trans. R. Soc. B Biol. Sci. 368, 13–16 (2013).
    Google Scholar 
    49.Prevéy, J. et al. Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob. Chang. Biol. 23, 2660–2671 (2017).ADS 
    PubMed 

    Google Scholar 
    50.Wipf, S. & Rixen, C. A review of snow manipulation experiments in Arctic and Alpine Tundra ecosystems. Polar Res. 29, 95–109 (2010).
    Google Scholar 
    51.Bokhorst, S. et al. Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Glob. Chang. Biol. 19, 64–74 (2013).ADS 
    PubMed 

    Google Scholar 
    52.Zhu, J., Zhang, Y. & Wang, W. Interactions between warming and soil moisture increase overlap in reproductive phenology among species in an alpine meadow. Biol. Lett. 12, 1–4 (2016).ADS 

    Google Scholar 
    53.Kemppinen, J., Niittynen, P., Aalto, J., le Roux, P. C. & Luoto, M. Water as a resource, stress and disturbance shaping tundra vegetation. Oikos 128, 811–822 (2019).
    Google Scholar 
    54.Panchen, Z. A. & Gorelick, R. Canadian arctic archipelago conspecifics flower earlier in the high arctic than the mid-arctic. Int. J. Plant Sci. 177, 661–670 (2016).
    Google Scholar 
    55.Barrett, R. T. & Hollister, R. D. Arctic plants are capable of sustained responses to long-term warming. Polar Res. 35, 1–9 (2016).
    Google Scholar 
    56.Carbognani, M., Bernareggi, G., Perucco, F., Tomaselli, M. & Petraglia, A. Micro-climatic controls and warming effects on flowering time in alpine snowbeds. Oecologia 182, 573–585 (2016).ADS 
    PubMed 

    Google Scholar 
    57.Hollister, R. D., Webber, P. J. & Tweedie, C. E. The response of Alaskan Arctic Tundra to experimental warming: Differences between short- and long-term responses. Glob. Chang. Biol. 11, 525–536 (2005).ADS 

    Google Scholar 
    58.Mulder, C. P. H., Iles, D. T. & Rockwell, R. F. Increased variance in temperature and lag effects alter phenological responses to rapid warming in a subarctic plant community. Glob. Chang. Biol. 23, 801–814 (2017).ADS 
    PubMed 

    Google Scholar 
    59.Marion, G. M. et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Chang. Biol. 3, 20–32 (1997).
    Google Scholar 
    60.Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl Acad. Sci. USA 103, 1342–1346 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    61.Hollister, R. D. & Webber, P. J. Biotic validation of small open-top chambers in a tundra ecosystem. Glob. Chang. Biol. 6, 835–842 (2000).ADS 

    Google Scholar 
    62.Henry, G. H. R. & Molau, U. Tundra plants and climate change: The International Tundra Experiment (ITEX). Glob. Chang. Biol. 3, 1–9 (1997).ADS 

    Google Scholar 
    63.Welker, J. M., Molau, U., Parsons, A. N., Robinson, C. H. & Wookey, P. A. Responses of Dryas octopetala to ITEX environmental manipulations: a synthesis with circumpolar comparisons. Glob. Chang. Biol. 3, 61–73 (1997).ADS 

    Google Scholar 
    64.Basnett, S., Nagaraju, S. K., Ravikanth, G. & Devy, S. M. Influence of phylogeny and abiotic factors varies across early and late reproductive phenology of Himalayan Rhododendrons. Ecosphere 10, e02581 (2019).65.Panchen, Z. A. et al. Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. N. Phytol. 203, 1208–1219 (2014).CAS 

    Google Scholar 
    66.Davis, C. C., Willis, C. G., Primack, R. B. & Miller-Rushing, A. J. The importance of phylogeny to the study of phenological response to global climate change. Philos. Trans. R. Soc. B Biol. Sci. 365, 3202–3213 (2010).
    Google Scholar 
    67.Hänninen, H. et al. Experiments are necessary in process-based tree phenology modelling. Trends Plant Sci. 24, 199–209 (2019).PubMed 

    Google Scholar 
    68.Hanson, P. J. & Walker, A. P. Advancing global change biology through experimental manipulations: Where have we been and where might we go? Glob. Chang. Biol. 26, 287–299 (2020).ADS 
    PubMed 

    Google Scholar 
    69.Tang, J. et al. Emerging opportunities and challenges in phenology: a review. Ecosphere 7, 1–17 (2016).
    Google Scholar 
    70.Ettinger, A. K. et al. Winter temperatures predominate in spring phenological responses to warming. Nat. Clim. Chang. 10, 1137–1142 (2020).71.Augspurger, C. K. Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing. Ecology 94, 41–50 (2013).PubMed 

    Google Scholar 
    72.Caradonna, P. J. & Bain, J. A. Frost sensitivity of leaves and fl owers of subalpine plants is related to tissue type and phenology. J. Ecol. 55–64 https://doi.org/10.1111/1365-2745.12482 (2016).73.Gezon, Z. J., Inouye, D. W. & Irwin, R. E. Phenological change in a spring ephemeral: Implications for pollination and plant reproduction. Glob. Chang. Biol. 22, 1779–1793 (2016).ADS 
    PubMed 

    Google Scholar 
    74.Iler, A. M. et al. Reproductive losses due to climate change-induced earlier flowering are not the primary threat to plant population viability in a perennial herb. J. Ecol. 107, 1931–1943 (2019).
    Google Scholar 
    75.CaraDonna, P. J. & Waser, N. M. Temporal flexibility in the structure of plant–pollinator interaction networks. Oikos 129, 1369–1380 (2020).
    Google Scholar 
    76.Fründ, J., Dormann, C. F. & Tscharntke, T. Linné’s floral clock is slow without pollinators – flower closure and plant-pollinator interaction webs. Ecol. Lett. 14, 896–904 (2011).PubMed 

    Google Scholar 
    77.Song, C. & Saavedra, S. Structural stability as a consistent predictor of phenological events. Proc. R. Soc. B Biol. Sci. 285, 20180767 (2018).78.Saavedra, S., Rohr, R. P., Olesen, J. M. & Bascompte, J. Nested species interactions promote feasibility over stability during the assembly of a pollinator community. Ecol. Evol. 6, 997–1007 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    79.Mosbacher, J. B., Michelsen, A., Stelvig, M., Hjermstad-Sollerud, H. & Schmidt, N. M. Muskoxen modify plant abundance, phenology, and nitrogen dynamics in a high Arctic Fen. Ecosystems 22, 1095–1107 (2019).
    Google Scholar 
    80.Barboza, P. S., Van Someren, L. L., Gustine, D. D. & Syndonia Bret-Harte, M. The nitrogen window for arctic herbivores: Plant phenology and protein gain of migratory caribou (Rangifer tarandus). Ecosphere 9, e02073 (2018).81.Gougherty, A. V. & Gougherty, S. W. Sequence of flower and leaf emergence in deciduous trees is linked to ecological traits, phylogenetics, and climate. N. Phytol. 220, 121–131 (2018).
    Google Scholar 
    82.Bjorkman, A. D. et al. Status and trends in Arctic vegetation: evidence from experimental warming and long-term monitoring. Ambio 49, 678–692 (2020).PubMed 

    Google Scholar 
    83.Loe, L. E. et al. The neglected season: Warmer autumns counteract harsher winters and promote population growth in Arctic reindeer. Glob. Chang. Biol. 993–1002 https://doi.org/10.1111/gcb.15458 (2020).84.Ueyama, M. et al. Growing season and spatial variations of carbon fluxes of Arctic and boreal ecosystems in Alaska (USA). Ecol. Appl. 23, 1798–1816 (2013).PubMed 

    Google Scholar 
    85.White, M. A., Running, S. W. & Thornton, P. E. The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int. J. Biometeorol. 42, 139–145 (1999).86.Natali, S. M. et al. Large loss of CO2 in winter observed across the northern permafrost region. Nat. Clim. Chang. 9, 852–857 (2019).ADS 
    CAS 

    Google Scholar 
    87.Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 3–7 (2008).
    Google Scholar 
    88.Radville, L., Post, E. & Eissenstat, D. M. On the sensitivity of root and leaf phenology to warming in the Arctic. Arctic Antarct. Alp. Res. 50, S100020 (2018).89.Sloan, V. L., Fletcher, B. J. & Phoenix, G. K. Contrasting synchrony in root and leaf phenology across multiple sub-Arctic plant communities. J. Ecol. 104, 239–248 (2016).CAS 

    Google Scholar 
    90.Danby, R. K. & Hik, D. S. Responses of white spruce (Picea glauca) to experimental warming at a subarctic alpine treeline. Glob. Chang. Biol. 13, 437–451 (2007).ADS 

    Google Scholar 
    91.Dabros, A., Fyles, J. W. & Strachan, I. B. Effects of open-top chambers on physical properties of air and soil at post-disturbance sites in northwestern Quebec. Plant Soil 333, 203–218 (2010).92.Finger Higgens, R. A. et al. Changing Lake Dynamics indicate a drier Arctic in Western Greenland. J. Geophys. Res. Biogeosci. 124, 870–883 (2019).
    Google Scholar 
    93.Leuzinger, S. et al. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol. Evol. 26, 236–241 (2011).PubMed 

    Google Scholar 
    94.Molau, U. & MØlgaard, P. ITEX Manual (1996).95.Post, E. et al. The polar regions in a 2 °C warmer world. Sci. Adv. 5, eaaw9883 (2019).96.Cayuela, L., Granzow-de la Cerda, Í., Albuquerque, F. S. & Golicher, D. J. Taxonstand: An r package for species names standardisation in vegetation databases. Methods Ecol. Evol. 3, 1078–1083 (2012).
    Google Scholar 
    97.C3S. ERA5: fifth generation of ECMWF atmospheric reanalyses of the global climate. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). https://cds.climate.copernicus.eu/cdsapp#!/home%0A (2017).98.Kittel, T. G. F. et al. Contrasting long-term alpine and subalpine precipitation trends in a mid-latitude North American mountain system, Colorado Front Range, USA. Plant Ecol. Divers. 8, 607–624 (2015).
    Google Scholar 
    99.Therneau, T. A package for survival analysis in S. Citeseer 1–83 (2020).100.R Core Team. R: A Language and Environment for Statistical Computing (2019).101.Bürkner, P.-C. brms: An R package for bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).102.van de Pol, M. & Wright, J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77, 753–758 (2009).
    Google Scholar 
    103.Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences linked references are available on JSTOR for this article: inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).MATH 

    Google Scholar 
    104.Makowski, D., Ben-Shachar, M. & Lüdecke, D. bayestestR: describing effects and their uncertainty, existence and significance within the Bayesian framework. J. Open Source Softw. 4, 1541 (2019).ADS 

    Google Scholar 
    105.Pebesma, E. Simple features for R: standardized support for spatial vector data. R J 10, 439–446 (2018).
    Google Scholar 
    106.Wickham, H. Elegant Graphics for Data Analysis Media Vol. 35 (Springer Publishing Company, Incorporated, 2009).107.Collins, C. cour10eygrace/OTC_synthesis_analyses: release for Nature Communications manuscript (Version v1.0.3). Zenodo https://doi.org/10.5281/zenodo.4763165 (2021). More

  • in

    Behavioral traits and territoriality in the symbiotic scaleworm Ophthalmonoe pettiboneae

    1.Baeza, J. A. & Thiel, M. Predicting territorial behavior in symbiotic crabs using host characteristics: A comparative study and proposal of a model. Mar. Biol. 142, 93–100. https://doi.org/10.1007/s00227-002-0927-1 (2003).Article 

    Google Scholar 
    2.Kamran, M. & Moore, P. A. Dominance and territory. In Encyclopedia of Evolutionary Psychological Science (eds Shackelford, T. K. & Weekes-Shackelford, V. A.) 1–4 (Springer, 2016).
    Google Scholar 
    3.Grant, J. W. A. Whether or not to defend? The influence of resource distribution. Mar. Behav. Physiol. 22, 137–153. https://doi.org/10.1080/10236249309378862 (1993).ADS 
    Article 

    Google Scholar 
    4.Duffy, J. E. The ecology and evolution of eusociality in sponge-dwelling shrimp. In Genes, Behaviors and Evolution of Social Insects (ed. Kikuchi, T.) 217–254 (Hokkaido University Press, 2002).
    Google Scholar 
    5.Baeza, J. A., Stotz, W. & Thiel, M. Agonistic behaviour and development of territoriality during ontogeny of the sea anemone dwelling crab Allopetrolisthes spinifrons (H. Milne Edwards, 1837)(Decapoda: Anomura: Porcellanidae). Mar. Freshw. Behav. Physiol. 35, 189–202. https://doi.org/10.1080/1023624021000003817 (2002).Article 

    Google Scholar 
    6.Castro, P. Symbiotic Brachyura. In Treatise on Zoology-Anatomy, Taxonomy, Biology. The Crustacea, Volume 9 Part C Vol. 2 (eds Castro, P. et al.) 543–581 (Brill, 2015).Chapter 

    Google Scholar 
    7.Wilson, E. O. Sociobiology: The New Synthesis (Harvard University, 1975).
    Google Scholar 
    8.Burt, W. H. Territoriality and home range concepts as applied to mammals. J. Mammal. 24, 346–352. https://doi.org/10.2307/1374834 (1943).Article 

    Google Scholar 
    9.Gerking, S. D. Feeding Ecology of Fish (Academic Press, 2014).
    Google Scholar 
    10.Barrows, E. M. Animal Behavior Desk Reference: A Dictionary of Animal Behavior, Ecology, and Evolution (CRC Press, 2000).Book 

    Google Scholar 
    11.Hardy, I. C. W. & Briffa, M. Animal Contests Vol. 357 (Cambridge University Press, 2013).Book 

    Google Scholar 
    12.Dimock, R. V. Jr. Intraspecific aggression and the distribution of a symbiotic polychaete on its host. In Symbiosis in the Sea (ed. Vernberg, W. B.) 29–44 (University of South Carolina Press, 1974).
    Google Scholar 
    13.Duffy, J. E., Morrison, C. L. & Macdonald, K. S. Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behav. Ecol. Sociobiol. 51, 488–495. https://doi.org/10.1007/s00265-002-0455-5 (2002).Article 

    Google Scholar 
    14.Huber, M. E. Aggressive behavior of Trapezia intermedia Miers and T. digitalis Latreille (Brachyura: Xanthidae). J. Crustacean Biol. 7, 238–248. https://doi.org/10.2307/1548604 (1987).Article 

    Google Scholar 
    15.Douglas, A. The Symbiotic Habit (Princeton University Press, 2010).
    Google Scholar 
    16.Williams, J. D. & McDermott, J. J. Hermit crab biocoenoses: A worldwide review of the diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 305, 1–128. https://doi.org/10.1016/j.jembe.2004.02.020 (2004).Article 

    Google Scholar 
    17.Fautin, D. G. The anemonefish symbiosis: What is known and what is not. Symbiosis 10, 23–46 (1991).
    Google Scholar 
    18.Martin, D. & Britayev, T. A. Symbiotic polychaetes: Review of known species. Oceanogr. Mar. Biol. Ann. Rev. 36, 217–340 (1998).
    Google Scholar 
    19.Fernández-Leborans, G. Epibiosis in Crustacea: An overview. Crustaceana 83, 549–640. https://doi.org/10.1163/001121610X532648 (2010).Article 

    Google Scholar 
    20.Stella, J. S., Pratchett, M. S., Hutchings, P. A. & Jones, G. P. Diversity, importance and vulnerability of coral-associated invertebrates. Oceanogr. Mar. Biol. Ann. Rev. 49, 43–116 (2011).
    Google Scholar 
    21.Thiel, M. & Baeza, J. A. Factors affecting the social behaviour of crustaceans living symbiotically with other marine invertebrates: a modelling approach. Symbiosis 30, 163–190 (2001).
    Google Scholar 
    22.Jones, K. M. M. The effect of territorial damselfish (family Pomacentridae) on the space use and behaviour of the coral reef fish Halichoeres bivittatus (Bloch, 1791) (family Labridae). J. Exp. Mar. Biol. Ecol. 324, 99–111. https://doi.org/10.1016/j.jembe.2005.04.009 (2005).Article 

    Google Scholar 
    23.Thiel, M., Zander, A. & Baeza, J. A. Movements of the symbiotic crab Liopetrolisthes mitra between its host sea urchin Tetrapygus niger. Bull. Mar. Sci. 72, 89–101 (2003).
    Google Scholar 
    24.Marin, I. & Britayev, T. A. Symbiotic Community Associated with Corals Galaxea Oken, 1815 (Euphillidae: Scleractinia) Vol. 148 (KMK Press, 2014).
    Google Scholar 
    25.Ross, R. M. Territorial behavior and ecology of the anemonefish Amphiprion melanopus on Guam. Z. Tierpsychol. 46, 71–83. https://doi.org/10.1111/j.1439-0310.1978.tb01439.x (1978).Article 

    Google Scholar 
    26.Kobayashi, M. & Hattori, A. Spacing pattern and body size composition of the protandrous anemonefish Amphiprion frenatus inhabiting colonial host anemones. Ichthyol. Res. 53, 1–6. https://doi.org/10.1007/s10228-005-0305-3 (2006).Article 

    Google Scholar 
    27.Huebner, L. K., Dailey, B., Titus, B. M., Khalaf, M. & Chadwick, N. E. Host preference and habitat segregation among Red Sea anemonefish: Effects of sea anemone traits and fish life stages. Mar. Ecol. Progr. Ser. 464, 1–15. https://doi.org/10.3354/meps09964 (2012).ADS 
    Article 

    Google Scholar 
    28.Duffy, J. E. Eusociality in a coral-reef shrimp. Nature 381, 512–514. https://doi.org/10.1038/381512a0 (1996).ADS 
    CAS 
    Article 

    Google Scholar 
    29.Baeza, J. A. & Stotz, W. B. Host-use pattern and host-selection during ontogeny of the commensal crab Allopetrolisthes spinifrons (H. Milne Edwards, 1837) (Decapoda: Anomura: Porcellanidae). J. Nat. Hist. 35, 341–355. https://doi.org/10.1080/002229301300009586 (2001).Article 

    Google Scholar 
    30.Ambrosio, L. J. & Baeza, J. A. Territoriality and conflict avoidance explain asociality (solitariness) of the endosymbiotic pea crab Tunicotheres moseri. PLoS ONE 11, e0148285–e0148285. https://doi.org/10.1371/journal.pone.0148285 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    31.Baeza, J. A. & Thiel, M. The mating system of symbiotic crustaceans: A conceptual model based on optimality and ecological constraints. In Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms (eds Duffy, J. E. & Thiel, M.) 250–267 (Oxford University Press, 2007).
    Google Scholar 
    32.Bell, J. L. Distribution and abundance of Dissodactylus mellitae Rathbun (Pinnotheridae) on Mellita quinquiesperforata (Leske)(Echinodermata). J. Exp. Mar. Biol. Ecol. 117, 93–114. https://doi.org/10.1016/0022-0981(88)90220-1 (1988).Article 

    Google Scholar 
    33.Castro, P. Movements between coral colonies in Trapezia ferruginea (Crustacea: Brachyura), an obligate symbiont of scleractinian corals. Mar. Biol. 46, 237–245. https://doi.org/10.1007/BF00390685 (1978).Article 

    Google Scholar 
    34.Baeza, J. A., Simpson, L., Ambrosio, L. J., Guéron, R. & Mora, N. Monogamy in a hyper-symbiotic shrimp. PLoS ONE 11, e0149797. https://doi.org/10.1371/journal.pone.0149797 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Diesel, R. Male-female association in the spider crab Inachus phalangium: The influence of female reproductive stage and size. J. Crustac. Biol. 8, 63–69. https://doi.org/10.1163/193724088X00080 (1988).Article 

    Google Scholar 
    36.Wells, H. W. & Wells, M. J. Observations on Pinnaxodes floridensis, a new species of pinnotherid crustacean commensal in holothurians. Bull. Mar. Sci. 11, 267–279 (1961).
    Google Scholar 
    37.Martin, D. & Britayev, T. A. Symbiotic polychaetes revisited: an update of the known species and relationships (1998–2017). Oceanogr. Mar. Biol. Ann. Rev. 56, 371–448. https://doi.org/10.1201/9780429454455-6 (2018).Article 

    Google Scholar 
    38.Perry, O., Sapir, Y., Perry, G., Ten Hove, H. & Fine, M. Substrate selection of Christmas tree worms (Spirobranchus spp.) in the Gulf of Eilat, Red Sea. J. Mar. Biol. Ass. UK 98, 791–799. https://doi.org/10.1017/S0025315416002022 (2018).Article 

    Google Scholar 
    39.Hunte, W., Colin, B. E. & Marsden, J. R. Habitat selection in the tropical polychaete Spirobranchus giganteus 1 Distribution on corals. Mar. Biol. 104, 87–92 (1990).Article 

    Google Scholar 
    40.Mackie, A. S. Y., Oliver, P. G. & Nygren, A. Antonbruunia sociabilis sp. nov (Annelida: Antonbruunidae) associated with the chemosynthetic deep-sea bivalve Thyasira scotiae Oliver & Drewery, 2014, and a re-examination of the systematic affinities of Antonbruunidae. Zootaxa 3995, 20–36 (2015).Article 

    Google Scholar 
    41.Ruff, R. E. A new species of Bathynoe (Polychaeta: Polynoidae) from the Northeast Pacific Ocean commensal with two species of deep-water asteroids. in: Systematics, Biology and Morphology of World Polychaeta. Proceedings of the Second International Polychaeta Conference. Ophelia Suppl. 5, 219–230 (1991).42.Miura, T. & Ohta, S. Two polychaete species from the deep-sea hydrothermal vent in the Middle Okinawa Trough. Zool. Sci. 8, 383–387 (1991).
    Google Scholar 
    43.Martin, D., Nygren, A., Hjelmstedt, P., Drake, P. & Gil, J. On the enigmatic symbiotic polychaete “Parasyllidea” humesi Pettibone, 1961 (Hesionidae): taxonomy, phylogeny and behaviour. Zool. J. Linn. Soc. 174, 429–446. https://doi.org/10.1111/zoj.12249 (2015).Article 

    Google Scholar 
    44.Chim, C. K., Ong, J. J. L. & Tan, K. S. An association between a hesionid polychaete and temnopleurid echinoids from Singapore. Cah. Biol. Mar. 54, 577–585. https://doi.org/10.21411/CBM.A.ED45E036 (2013).Article 

    Google Scholar 
    45.Goerke, H. Nereis fucata (Polychaeta, Nereidae) als kommensale von Eupagurus bernhardus (Crustacea, Decapoda) Entwicklung einer population und verhalten der art. Veröffentlichungen des Instituts für Meeresforschung in Bremerhaven 13, 79–81 (1971).
    Google Scholar 
    46.Britayev, T. A., Mekhova, E., Deart, Y. & Martin, D. Do syntopic host species harbour similar symbiotic communities? The case of Chaetopterus spp. (Annelida: Chaetopteridae). PeerJ 5, e2930. https://doi.org/10.7717/peerj.2930 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    47.Britayev, T. A., Martin, D., Krylova, E. M., von Cosel, R. & Aksiuk, E. S. Life-history traits of the symbiotic scale-worm Branchipolynoe seepensis and its relationships with host mussels of the genus Bathymodiolus from hydrothermal vents. Mar. Ecol. Evolut. Perspect. 28, 36–48. https://doi.org/10.1111/j.1439-0485.2007.00152.x (2007).Article 

    Google Scholar 
    48.Britayev, T. A. & Zamyshliak, E. A. Association of the commensal scaleworm Gastrolepidia clavigera (Polychaeta: Polynoidae) with holothurians near the coast of South Vietnam. Ophelia 45, 175–190 (1996).Article 

    Google Scholar 
    49.Britayev, T. A. Life cycle of the symbiotic scale-worm Arctonoe vittata (Polychaeta: Polynoidae). In: Systematics, Biology and Morphology of World Polychaeta. Proceedings of the Second International Polychaeta Conference. Ophelia Suppl. 5, 305–312 (1991).50.Devaney, D. M. An ectocommensal polynoid associated with Indo-pacific echinoderms, primarily ophiuroids. Occ. Pap. Bernice P. Bishop Mus. 23, 287–304 (1967).
    Google Scholar 
    51.Tokaji, H., Nakahara, K. & Goshima, S. Host switching improves survival rate of the symbiotic polychaete Arctonoe vittata. Plank. Bent. Res. 9, 189–196. https://doi.org/10.3800/pbr.9.189 (2014).Article 

    Google Scholar 
    52.Martin, D., Rosell, D. & Uriz, M. J. Harmothoe hyalonemae sp. nov. (Polychaeta, Polynoidae), an exclusive inhabitant of different Atlanto-Mediterranean species of Hyalonema (Porifera, Hexactinellida). Ophelia 35, 169–185 (1992).Article 

    Google Scholar 
    53.Reish, D. J. & Alosi, M. C. Aggressive behavior in the polychaetous annelid family Nereidae. Bull. South. Calif. Acad. Sci. 67, 21–28 (1968).
    Google Scholar 
    54.Evans, S. M. Behavior in polychaetes. Q. Rev. Biol. 46, 379–405 (1971).Article 

    Google Scholar 
    55.Scaps, P. Intraspecific agonistic behaviour in the polychaete Perinereis cultrifera (Grübe). Vie et Milieu 45, 123–128 (1995).
    Google Scholar 
    56.Johnson, H. P. A preliminary account of the marine annelids of the Pacific coast, with descriptions of new species. Proc. Calif. Acad. Sci. 1, 153–199 (1897).
    Google Scholar 
    57.Miers, E. J. Report on the Brachyura collected by HMS Challenger during the years 1873–1876. in: Report on the scientific results of the Voyage of HMS Challenger during the years 1873–76 under the command of Captain George S. Nares, R. N., F.R.S. and the late Captain Frank Tourle Thompson, R. N. Zoology 17, 1–363, pls. 361–329 (1886).58.Latreille, P. A. Trapezie. in Entomologie, ou histoire naturelle des crustaces, des arachnides et des insectes, Vol. 10 695–696 (Encyclopedie Methodique, Histoire Naturelle, 1828).59.Petersen, M. E. & Britayev, T. A. A new genus and species of polynoid scaleworm commensal with Chaetopterus appendiculatus Grube from the Banda Sea (Annelida: Polychaeta), with a review of commensals of Chaetopteridae. Bull. Mar. Sci. 60, 261–276 (1997).
    Google Scholar 
    60.Grube, A. E. Descriptiones Annulatorum novorum mare Ceylonicum habitantium ab honoratissimo Holdsworth collectorum. Proc. Zool. Soc. Lond. 41, 325–329. https://doi.org/10.1111/j.1096-3642.1874.tb02492.x (1874).Article 

    Google Scholar 
    61.Britayev, T. A. & Martin, D. Scale-worms (Polychaeta, Polynoidae) associated with chaetopterid worms (Polychaeta, Chaetopteridae), with description of a new genus and species. J. Nat. Hist. 39, 4081–4099. https://doi.org/10.1080/00222930600556229 (2005).Article 

    Google Scholar 
    62.Grant, J. W. A., Gaboury, C. L. & Levitt, H. L. Competitor-to-resource ratio, a general formulation of operational sex ratio, as a predictor of competitive aggression in Japanese medaka (Pisces: Oryziidae). Behav. Ecol. 11, 670–675. https://doi.org/10.1093/beheco/11.6.670 (2000).Article 

    Google Scholar 
    63.Britayev, T. A. & Smurov, A. V. Distribution and relocation of commensal crabs Pinnixa rathbhuni (Pinnotheridae) on their hosts. Dokl. Akad. Nauk SSSR 300, 1506–1509 (1988).
    Google Scholar 
    64.Walker, A. O. Notes on a collection of Crustacea from Singapore. J. Linn. Soc. Lond. Zool. 20, 107–117. https://doi.org/10.1111/j.1096-3642.1887.tb01440.x (1887).Article 

    Google Scholar 
    65.Kemp, D. J. Habitat selection and territoriality. In Insect behavior: from mechanisms to ecological and evolutionary consequences (eds Córdoba-Aguilar, A. et al.) 80–97 (Oxford University Press, 2018).
    Google Scholar 
    66.Jumars, P. A., Dorgan, K. M. & Lindsay, S. M. Diet of worms emended: An update of polychaete feeding guilds. Ann. Rev. Mar. Sci. 7, 497–520. https://doi.org/10.1146/annurev-marine-010814-020007 (2015).Article 
    PubMed 

    Google Scholar 
    67.Cotter, E., O’Riordan, R. M. & Myers, A. A. A histological study of reproduction in the serpulids Pomatoceros triqueter and Pomatoceros lamarckii (Annelida: Polychaeta). Mar. Biol. 142, 905–914 (2003).Article 

    Google Scholar 
    68.Prevedelli, D., Massamba N’Siala, G., Ansaloni, I. & Simonini, R. Life cycle of Marphysa sanguinea (Polychaeta: Eunicidae) in the Venice Lagoon (Italy). Mar. Ecol. 28, 384–393. https://doi.org/10.1111/j.1439-0485.2007.00160.x (2007).ADS 
    Article 

    Google Scholar 
    69.Bergman, D. A. & Moore, P. A. Prolonged exposure to social odours alters subsequent social interactions in crayfish (Orconectes rusticus). Anim. Behav. 70, 311–318. https://doi.org/10.1016/j.anbehav.2004.10.026 (2005).Article 

    Google Scholar 
    70.Arakaki, J. Y. et al. Battle of the borders: Is a range-extending fiddler crab affecting the spatial niche of a congener species?. J. Exp. Mar. Biol. Ecol. 532, 151445. https://doi.org/10.1016/j.jembe.2020.151445 (2020).Article 

    Google Scholar 
    71.Britayev, T. A. & Mekhova, E. S. Do symbiotic polychaetes migrate from host to host?. Mem. Mus. Victoria 71, 21–25 (2014).Article 

    Google Scholar 
    72.Livermore, J., Perreault, T. & Rivers, T. Luminescent defensive behaviors of polynoid polychaete worms to natural predators. Mar. Biol. 165, 149. https://doi.org/10.1007/s00227-018-3403-2 (2018).Article 

    Google Scholar 
    73.Daly, J. M. Segmentation, autotomy and regeneration of lost posterior segments in Harmothoe imbricata (L) (Polychaeta: Polynoidae). QH1.M454 1, 17–28 (1973).
    Google Scholar 
    74.Schiaparelli, S., Alvaro, M. C. & Barnich, R. Polynoid polychaetes living in the gut of irregular sea urchins: A first case of inquilinism in the Southern Ocean. Antarct. Sci. 23, 144–151. https://doi.org/10.1017/S0954102011000083 (2011).ADS 
    Article 

    Google Scholar 
    75.Sokal, R. R. & Rohlf, F. J. Biometry. The Principles and Practice of Statistics in Biological Research 3rd edn. (W.H. Freeman and Company, 1995).MATH 

    Google Scholar 
    76.Everitt, B. The Analysis of Contingency Tables 2nd edn. (Chapman & Hall, 1992).Book 

    Google Scholar  More

  • in

    Transcriptional response to prolonged perchlorate exposure in the methanogen Methanosarcina barkeri and implications for Martian habitability

    1.Krasnopolsky, V. A., Maillard, J. P. & Owen, T. C. Detection of methane in the martian atmosphere: evidence for life?. Icarus 172, 537–547 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    2.Formisano, V., Atreya, S., Encrenaz, T., Ignatiev, N. & Giuranna, M. Detection of methane in the atmosphere of mars. Science 306, 1758–1761 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Geminale, A., Formisano, V. & Giuranna, M. Methane in Martian atmosphere: average spatial, diurnal, and seasonal behaviour. Planet. Space Sci. 56, 1194–1203 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Mumma, M. J. et al. Strong release of methane on mars in northern summer 2003. Science 323, 1041–1045 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Webster, C. R. et al. Mars methane detection and variability at Gale crater. Science 347, 415–417 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Webster, C. R. et al. Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 360, 1093–1096 (2018).ADS 
    MathSciNet 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Korablev, O. et al. No detection of methane on Mars from early ExoMars Trace Gas Orbiter observations. Nature 568, 517–520 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Fries, M. et al. A cometary origin for martian atmospheric methane. Geochem. Perspect. Lett. 2, 10–23 (2016).Article 

    Google Scholar 
    9.Keppler, F. et al. Ultraviolet-radiation-induced methane emissions from meteorites and the Martian atmosphere. Nature 486, 93–96 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Moores, J. E. & Schuerger, A. C. UV degradation of accreted organics on Mars: IDP longevity, surface reservoir of organics, and relevance to the detection of methane in the atmosphere. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    11.Schuerger, A. C., Moores, J. E., Clausen, C. A., Barlow, N. G. & Britt, D. T. Methane from UV-irradiated carbonaceous chondrites under simulated Martian conditions. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    12.Etiope, G., Ehlmann, B. L. & Schoell, M. Low temperature production and exhalation of methane from serpentinized rocks on Earth: a potential analog for methane production on Mars. Icarus 224, 276–285 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    13.Oehler, D. Z. & Etiope, G. Methane seepage on mars: where to look and why. Astrobiology 17, 1233–1264 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Onstott, T. C. et al. Martian CH 4: sources, flux, and detection. Astrobiology 6, 377–395 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Elwood Madden, M. E., Ulrich, S. M., Onstott, T. C. & Phelps, T. J. Salinity-induced hydrate dissociation: A mechanism for recent CH4 release on Mars. Geophys. Res. Lett. https://doi.org/10.1029/2006GL029156 (2007).Article 

    Google Scholar 
    16.Conrad, R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ. Microbiol. Rep. 1, 285–292 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Kendrick, M. G. & Kral, T. A. Survival of methanogens during desiccation: implications for life on mars. Astrobiology 6, 546–551 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Anderson, K. L., Apolinario, E. E. & Sowers, K. R. Desiccation as a long-term survival mechanism for the archaeon Methanosarcina barkeri. Appl. Environ. Microbiol. 78, 1473–1479 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Kral, T. A. & Altheide, S. T. Methanogen survival following exposure to desiccation, low pressure and martian regolith analogs. Planet. Space Sci. 89, 167–171 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    20.Sowers, K. R. & Gunsalus, R. P. Adaptation for growth at various saline concentrations by the archaebacterium Methanosarcina thermophila. J. Bacteriol. 170, 998–1002 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Maestrojuan, G. M. et al. Taxonomy and halotolerance of mesophilic methanosarcina strains, assignment of strains to species, and synonymy of methanosarcina mazei and methanosarcina frisia. Int. J. Syst. Bacteriol. 42, 561–567 (1992).CAS 
    Article 

    Google Scholar 
    22.Sowers, K. R., Boone, J. E. & Gunsalus, R. P. Disaggregation of methanosarcina spp and growth as single cells at elevated osmolarity. Appl. Environ. Microbiol. 59, 3832–3839 (1993).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Sowers, K. R. & Gunsalus, R. P. Halotolerance in methanosarcina spp: Role of N(sup(epsilon))-Acetyl-(beta)-Lysine, (alpha)-Glutamate, Glycine Betaine, and K(sup+) as Compatible Solutes for Osmotic Adaptation. Appl. Environ. Microbiol. 61, 4382–4388 (1995).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Roessler, M. et al. Identification of a salt-induced primary transporter for glycine betaine in the methanogen methanosarcina mazei go1. Appl. Environ. Microbiol. 68, 2133–2139 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Shcherbakova, V., Oshurkova, V. & Yoshimura, Y. The effects of perchlorates on the permafrost methanogens: implication for autotrophic life on mars. Microorganisms 3, 518–534 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Kral, T. A. et al. Sensitivity and adaptability of methanogens to perchlorates: Implications for life on Mars. Planet. Space Sci. 120, 87–95 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Rivkina, E. M., Laurinavichus, K. S., Gilichinsky, D. A. & Shcherbakova, V. A. Methane generation in permafrost sediments. Dokl. Biol. Sci. https://doi.org/10.1023/A:1015366613580 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Rivkina, E. et al. Microbial life in permafrost. Adv. Sp. Res. 33, 1215–1221 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    29.Rivkina, E. et al. Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol. Ecol. 61, 1–15 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Takai, K. et al. Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. U. S. A. 105, 10949–10954 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Sinha, N., Nepal, S., Kral, T. & Kumar, P. Survivability and growth kinetics of methanogenic archaea at various pHs and pressures: implications for deep subsurface life on Mars. Planet. Space Sci. 136, 15–24 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    32.Chastain, B. K. & Kral, T. A. Approaching mars-like geochemical conditions in the laboratory: omission of artificial buffers and reductants in a study of biogenic methane production on a Smectite clay. Astrobiology 10, 889–897 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Kral, T. A., Altheide, T. S., Lueders, A. E. & Schuerger, A. C. Low pressure and desiccation effects on methanogens: Implications for life on Mars. Planet. Space Sci. 59, 264–270 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Mickol, R. L. & Kral, T. A. Low pressure tolerance by methanogens in an aqueous environment: implications for subsurface life on mars. Orig. Life Evol. Biosph. 47, 511–532 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nat. Rev. Microbiol. 2, 569–580 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Ericksen, G. E. The Chilean Nitrate Deposits: The origin of the Chilean nitrate deposits, which contain a unique group of saline minerals, has provoked lively discussion for more than 100 years. Am. Sci. 71, 366–374 (1983).ADS 

    Google Scholar 
    37.Kounaves, S. P. et al. Discovery of natural perchlorate in the antarctic dry valleys and its global implications. Environ. Sci. Technol. 44, 2360–2364 (2010).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Hecht, M. H. et al. Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science 325, 64–67 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Navarro-González, R., Vargas, E., de la Rosa, J., Raga, A. C. & McKay, C. P. Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars. J. Geophys. Res. 115, E12010 (2010).ADS 
    Article 

    Google Scholar 
    40.Glavin, D. P. et al. Evidence for perchlorates and the origin of chlorinated hydrocarbons detected by SAM at the Rocknest aeolian deposit in Gale Crater. J. Geophys. Res. Planets 118, 1955–1973 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Kounaves, S. P. et al. Identification of the perchlorate parent salts at the Phoenix Mars landing site and possible implications. Icarus 232, 226–231 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    42.Kounaves, S. P., Carrier, B. L., O’Neil, G. D., Stroble, S. T. & Claire, M. W. Evidence of martian perchlorate, chlorate, and nitrate in Mars meteorite EETA79001: Implications for oxidants and organics. Icarus 229, 206–213 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    43.Ojha, L. et al. Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat. Geosci. https://doi.org/10.1038/ngeo2546 (2015).Article 

    Google Scholar 
    44.Clark, B. C. & Kounaves, S. P. Evidence for the distribution of perchlorates on Mars. Int. J. Astrobiol. 15, 311–318 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Pestova, O. N., Myund, L. A., Khripun, M. K. & Prigaro, A. V. Polythermal study of the systems M(ClO4)2–H2O (M2+ = Mg2+, Ca2+, Sr2+, Ba2+). Russ. J. Appl. Chem. 78, 409–413 (2005).CAS 
    Article 

    Google Scholar 
    46.Chevrier, V. F., Hanley, J. & Altheide, T. S. Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site Mars. Geophys. Res. Lett. 36, L10202 (2009).ADS 
    Article 
    CAS 

    Google Scholar 
    47.Marion, G. M., Catling, D. C., Zahnle, K. J. & Claire, M. W. Modeling aqueous perchlorate chemistries with applications to Mars. Icarus 207, 675–685 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    48.Stillman, D. E. & Grimm, R. E. Dielectric signatures of adsorbed and salty liquid water at the Phoenix landing site Mars. J. Geophys. Res. 116, E09005 (2011).ADS 

    Google Scholar 
    49.Toner, J. D., Catling, D. C. & Light, B. The formation of supercooled brines, viscous liquids, and low-temperature perchlorate glasses in aqueous solutions relevant to Mars. Icarus 233, 36–47 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    50.Nikolakakos, G. & Whiteway, J. A. Laboratory investigation of perchlorate deliquescence at the surface of Mars with a Raman scattering lidar. Geophys. Res. Lett. 42, 7899–7906 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    51.Maeder, D. L. et al. The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes. J. Bacteriol. 188, 7922–7931 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Sorek, R. & Cossart, P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat. Rev. Genet. 11, 9–16 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Lobo, A. L. & Zinder, S. H. Diazotrophy and Nitrogenase Activity in the Archaebacterium Methanosarcina barkeri 227. Appl. Environ. Microbiol. 54, 1656–1661 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Lobo, A. L. & Zinder, S. H. Nitrogenase in the archaebacterium Methanosarcina barkeri 227. J. Bacteriol. 172, 6789–6796 (1990).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Kessler, P. S. & Leigh, J. A. Genetics of nitrogen regulation in Methanococcus maripaludis. Genetics 152, 1343–1351 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Kessler, P. S., Daniel, C. & Leigh, J. A. Ammonia Switch-Off of Nitrogen Fixation in the Methanogenic Archaeon Methanococcus maripaludis: Mechanistic Features and Requirement for the Novel GlnB Homologues, NifI1 and NifI2. J. Bacteriol. 183, 882–889 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Kempf, B. & Bremer, E. OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in bacillus subtilis. J. Biol. Chem. 270, 16701–16713 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Kempf, B. & Bremer, E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319–330 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Hoffmann, T. & Bremer, E. Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol. Chem. 398, 193–214 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Hippe, H., Caspari, D., Fiebig, K. & Gottschalk, G. Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Proc. Natl. Acad. Sci. 76, 494–498 (1979).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Kreisl, P. & Kandler, O. Chemical structure of the cell wall polymer of methanosarcina. Syst. Appl. Microbiol. 7, 293–299 (1986).CAS 
    Article 

    Google Scholar 
    62.Jarrell, K. F., Jones, G. M., Kandiba, L., Nair, D. B. & Eichler, J. S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications. Archaea 2010, 1–13 (2010).Article 
    CAS 

    Google Scholar 
    63.Srinivasan, G. Pyrrolysine encoded by UAG in archaea: charging of a UAG-decoding specialized tRNA. Science 296, 1459–1462 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Bin, P., Huang, R. & Zhou, X. Oxidation resistance of the sulfur amino acids: methionine and cysteine. Biomed Res. Int. 2017, 1–6 (2017).Article 
    CAS 

    Google Scholar 
    65.Armesto, X. L., Canle, L. M., Fernández, M. I., Garcı́a, M. V. & Santaballa, J. A. First steps in the oxidation of sulfur-containing amino acids by hypohalogenation: very fast generation of intermediate sulfenyl halides and halosulfonium cations. Tetrahedron 56, 1103–1109 (2000).CAS 
    Article 

    Google Scholar 
    66.Casanueva, A., Tuffin, M., Cary, C. & Cowan, D. A. Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol. 18, 374–381 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Oren, A. Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie Van Leeuwenhoek 58, 291–298 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Seibel, B. A. & Walsh, P. J. Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol. 205, 297–306 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Lobo, A. L. & Zinder, S. H. Nitrogen fixation by methanogenic bacteria. in Biological Nitrogen Fixation (eds. Stacey, G., Burris, R. H. & Evans, H. J.) 191–211 (Chapman and Hall, 1992).70.Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9, 499–508 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Bardiya, N. & Bae, J.-H. Dissimilatory perchlorate reduction: A review. Microbiol. Res. 166, 237–254 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Barnum, T. P. et al. Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities. ISME J. 12, 1568–1581 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Oren, A., Elevi, B. R. & Mana, L. Perchlorate and halophilic prokaryotes: implications for possible halophilic life on Mars. Extremophiles 18, 75–80 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Liebensteiner, M. G., Pinkse, M. W. H., Schaap, P. J., Stams, A. J. M. & Lomans, B. P. Archaeal (Per)Chlorate reduction at high temperature: an interplay of biotic and abiotic reactions. Science 340, 85–87 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    75.Bender, K. S. et al. Identification, characterization, and classification of genes encoding perchlorate reductase. J. Bacteriol. 187, 5090–5096 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Youngblut, M. D. et al. Perchlorate reductase is distinguished by active site aromatic gate residues. J. Biol. Chem. 291, 9190–9202 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Okeke, B. C., Giblin, T. & Frankenberger, W. T. Reduction of perchlorate and nitrate by salt tolerant bacteria. Environ. Pollut. https://doi.org/10.1016/S0269-7491(01)00288-3 (2002).Article 
    PubMed 

    Google Scholar 
    78.He, L. et al. Biological perchlorate reduction: which electron donor we can choose?. Environ. Sci. Pollut. Res. 26, 16906–16922 (2019).CAS 
    Article 

    Google Scholar 
    79.Xie, T. et al. Perchlorate bioreduction linked to methane oxidation in a membrane biofilm reactor: performance and microbial community structure. J. Hazard. Mater. https://doi.org/10.1016/j.jhazmat.2018.06.011 (2018).Article 
    PubMed 

    Google Scholar 
    80.Chaudhuri, S. K., O’Connor, S. M., Gustavson, R. L., Achenbach, L. A. & Coates, J. D. Environmental factors that control microbial perchlorate reduction. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.68.9.4425-4430.2002 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Abu-Omar, M. M. Effective and catalytic reduction of perchlorate by atom transfer-reaction kinetics and mechanisms. Comments Inorg. Chem. 24, 15–37 (2003).CAS 
    Article 

    Google Scholar 
    82.Adkins, H. & Cramer, H. I. The use of nickel as a catalyst for hydrogenation. J. Am. Chem. Soc. 52, 4349–4358 (1930).CAS 
    Article 

    Google Scholar 
    83.Thauer, R. K. et al. Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu. Rev. Biochem. 79, 507–536 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Zhang, H., Bruns, M. A. & Logan, B. E. Perchlorate reduction by a novel chemolithoautotrophic, hydrogen-oxidizing bacterium. Environ. Microbiol. https://doi.org/10.1046/j.1462-2920.2002.00338.x (2002).Article 
    PubMed 

    Google Scholar 
    85.Ide, T., Bäumer, S. & Deppenmeier, U. Energy conservation by the H2: heterodisulfide oxidoreductase from methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol. 181, 4076–4080 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Deppenmeier, U. The membrane-bound electron transport system of methanosarcina species. J. Bioenerg. Biomembr. 36, 55–64 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R. & Metcalf, W. W. Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc. Natl. Acad. Sci. 99, 5632–5637 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Kulkarni, G., Mand, T. D. & Metcalf, W. W. Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri. MBio 9, (2018).89.Bobik, T. Formyl-methanofuran synthesis in Methanobacterium thermoautotrophicum. FEMS Microbiol. Lett. 87, 323–326 (1990).CAS 
    Article 

    Google Scholar 
    90.Wang, D. M., Shah, S. I., Chen, J. G. & Huang, C. P. Catalytic reduction of perchlorate by H2 gas in dilute aqueous solutions. Sep. Purif. Technol. 60, 14–21 (2008).CAS 
    Article 

    Google Scholar 
    91.Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579–591 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    92.Mand, T. D. & Metcalf, W. W. Energy Conservation and Hydrogenase Function in Methanogenic Archaea, in Particular the Genus Methanosarcina. Microbiol. Mol. Biol. Rev. 83, (2019).93.Rummel, J. D. et al. A new analysis of mars “special regions”: findings of the second MEPAG special regions science analysis group (SR-SAG2). Astrobiology 14, 887–968 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    94.Bryant, M. P. & Boone, D. R. Emended description of strain MST(DSM 800T), the type strain of methanosarcina barkeri. Int. J. Syst. Bacteriol. 37, 169–170 (1987).Article 

    Google Scholar 
    95.Widdel, F., Kohring, G.-W. & Mayer, F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Arch. Microbiol. 134, 286–294 (1983).CAS 
    Article 

    Google Scholar 
    96.Francisco, D. E., Mah, R. A. & Rabin, A. C. Acridine orange-epifluorescence technique for counting bacteria in natural waters. Trans. Am. Microsc. Soc. 92, 416 (1973).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

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

    Google Scholar 
    99.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    100.Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    101.Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    102.Love, M., Anders, S. & Huber, W. Differential analysis of count data–the DESeq2 package. Genome Biol. 15, 10–1186 (2014).Article 
    CAS 

    Google Scholar 
    103.Ogata, H. et al. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27, 29–34 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish

    1.Clobert, J., Baguette, M., Benton, T. G. & Bullock, J. M. Dispersal Ecology and Evolution (Oxford University Press, 2012).Book 

    Google Scholar 
    2.Paris, C. B. & Cowen, R. K. Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol. Oceanogr. 49, 1964–1979 (2004).ADS 
    Article 

    Google Scholar 
    3.Roberts, C. M. Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457 (1997).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Fisher, R. & Wilson, S. K. Maximum sustainable swimming speeds of late-stage larvae of nine species of reef fishes. J. Exp. Mar. Biol. Ecol. 312, 171–186 (2004).Article 

    Google Scholar 
    5.Fisher, R., Leis, J. M., Clark, D. L. & Wilson, S. K. Critical swimming speeds of late-stage coral reef fish larvae: variation within species, among species and between locations. Mar. Biol. 147, 1201–1212 (2005).Article 

    Google Scholar 
    6.Leis, J. M. Ontogeny of behaviour in larvae of marine demersal fishes. Ichthyol. Res. 57, 325–342 (2010).Article 

    Google Scholar 
    7.Faillettaz, R., Durand, E., Paris, C. B., Koubbi, P. & Irisson, J.-O. Swimming speeds of Mediterranean settlement-stage fish larvae nuance Hjort’s aberrant drift hypothesis. Limnol. Oceanogr. 63, 509–523 (2018).ADS 
    Article 

    Google Scholar 
    8.Majoris, J. E., Catalano, K. A., Scolaro, D., Atema, J. & Buston, P. M. Ontogeny of larval swimming abilities in three species of coral reef fishes and a hypothesis for their impact on the spatial scale of dispersal. Mar. Biol. 166, 159 (2019).Article 

    Google Scholar 
    9.Leis, J. M., Sweatman, H. P. & Reader, S. E. What the pelagic stages of coral reef fishes are doing out in blue water: daytime field observations of larval behavioural capabilities. Mar. Freshw. Res. 47, 401–411 (1996).Article 

    Google Scholar 
    10.Leis, J., Paris, C., Irisson, J., Yerman, M. & Siebeck, U. Orientation of fish larvae in situ is consistent among locations, years and methods, but varies with time of day. Mar. Ecol. Prog. Ser. 505, 193–208 (2014).ADS 
    Article 

    Google Scholar 
    11.Leis, J. M. & Carson-Ewart, B. M. Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar. Ecol. Prog. Ser. 252, 239–253 (2003).ADS 
    Article 

    Google Scholar 
    12.Paris, C. B., Guigand, C. M., Irisson, J.-O., Fisher, R. & D’Alessandro, E. Orientation with no frame of reference (OWNFOR): a novel system to observe and quantify orientation in reef fish larvae. In Caribbean Connectivity: Implications for Marine Protected Area Management 52–62 (2008).13.Rossi, A., Irisson, J.-O., Levaray, M., Pasqualini, V. & Agostini, S. Orientation of Mediterranean fish larvae varies with location. Mar. Biol. 166, 100 (2019).Article 

    Google Scholar 
    14.Simpson, S. D., Meekan, M., Montgomery, J., McCauley, R. & Jeffs, A. Homeward sound. Science 308, 221–221 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Leis, J. M., Siebeck, U. & Dixson, D. L. How nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integr. Comp. Biol. 51, 826–843 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Paris, C. B. et al. Reef odor: a wake up call for navigation in reef fish larvae. PLoS ONE 8, e72808 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Mouritsen, H., Atema, J., Kingsford, M. J. & Gerlach, G. Sun compass orientation helps coral reef fish larvae return to their natal reef. PLoS ONE 8, e66039 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Berenshtein, I. et al. Polarized light sensitivity and orientation in coral reef fish post-larvae. PLoS ONE 9, e88468 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    19.Bottesch, M. et al. A magnetic compass that might help coral reef fish larvae return to their natal reef. Curr. Biol. 26, R1266–R1267 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Cresci, A., Allan, B. J. M., Shema, S. D., Skiftesvik, A. B. & Browman, H. I. Orientation behavior and swimming speed of Atlantic herring larvae (Clupea harengus) in situ and in laboratory exposures to rotated artificial magnetic fields. J. Exp. Mar. Biol. Ecol. 526, 151358 (2020).Article 

    Google Scholar 
    21.Faillettaz, R., Paris, C. B. & Irisson, J.-O. Larval fish swimming behavior alters dispersal patterns from marine protected areas in the North-Western Mediterranean Sea. Front. Mar. Sci. 5, 97 (2018).Article 

    Google Scholar 
    22.Staaterman, E., Paris, C. B. & Helgers, J. Orientation behavior in fish larvae: a missing piece to Hjort’s critical period hypothesis. J. Theor. Biol. 304, 188–196 (2012).PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 
    23.Lara, M. R. Development of the nasal olfactory organs in the larvae, settlement-stages and some adults of 14 species of Caribbean reef fishes (Labridae, Scaridae, Pomacentridae). Mar. Biol. 154, 51–64 (2008).Article 

    Google Scholar 
    24.Arvedlund, M. & Kavanagh, K. The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems. In Ecological Connectivity among Tropical Coastal Ecosystems (ed. Nagelkerken, I.) 135–184 (Springer, 2009).Chapter 

    Google Scholar 
    25.Teodósio, M. A., Paris, C. B., Wolanski, E. & Morais, P. Biophysical processes leading to the ingress of temperate fish larvae into estuarine nursery areas: a review. Estuar. Coast. Shelf Sci. 183, 187–202 (2016).ADS 
    Article 

    Google Scholar 
    26.Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology. J. Fish Biol. 95, 311–323 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Nickles, K. R., Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Organization and ontogeny of a complex lateral line system in a Goby (Elacatinus lori), with a consideration of function and ecology. Copeia 108, 863–885 (2020).Article 

    Google Scholar 
    28.Fuiman, L., Higgs, D. & Poling, K. Changing structure and function of the ear and lateral line system of fishes during development. Am. Fish. Soc. Symp. 2004, 117–144 (2004).
    Google Scholar 
    29.Blaxter, J. H. S. Light intensity, vision, and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293–307 (1968).Article 

    Google Scholar 
    30.Blaxter, J. H. S. & Hoss, D. E. The effect of rapid changes of hydrostatic pressure on the Atlantic herring Clupea harengus L. II. The response of the auditory bulla system in larvae and juveniles. J. Exp. Mar. Biol. Ecol. 41, 87–100 (1979).Article 

    Google Scholar 
    31.Colin, P. L. A new species of sponge-dwelling Elacatinus (Pisces: Gobiidae) from the western Caribbean. Zootaxa 106, 1–7 (2002).Article 

    Google Scholar 
    32.Colin, P. L. Fishes as living tracers of connectivity in the tropical western North Atlantic: I. Distribution of the neon gobies, genus Elacatinus (Pisces: Gobiidae). Zootaxa 2370, 36–52 (2010).Article 

    Google Scholar 
    33.Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.D’Aloia, C. C., Majoris, J. E. & Buston, P. M. Predictors of the distribution and abundance of a tube sponge and its resident goby. Coral Reefs 30, 777 (2011).ADS 
    Article 

    Google Scholar 
    35.Majoris, J. E., Francisco, F. A., Atema, J. & Buston, P. M. Reproduction, early development, and larval rearing strategies for two sponge-dwelling neon gobies, Elacatinus lori and E. colini. Aquaculture 483, 286–295 (2018).Article 

    Google Scholar 
    36.D’Aloia, C. C. et al. Patterns, causes, and consequences of marine larval dispersal. Proc. Natl. Acad. Sci. 112, 13940–13945 (2015).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    37.Majoris, J. E., D’Aloia, C. C., Francis, R. K. & Buston, P. M. Differential persistence favors habitat preferences that determine the distribution of a reef fish. Behav. Ecol. 29, 429–439 (2018).Article 

    Google Scholar 
    38.Chaput, R., Majoris, J. E., Guigand, C. M., Huse, M. & D’Alessandro, E. K. Environmental conditions and paternal care determine hatching synchronicity of coral reef fish larvae. Mar. Biol. 166, 118 (2019).Article 
    CAS 

    Google Scholar 
    39.D’Aloia, C., Xuereb, A., Fortin, M., Bogdanowicz, S. & Buston, P. Limited dispersal explains the spatial distribution of siblings in a reef fish population. Mar. Ecol. Prog. Ser. 607, 143–154 (2018).ADS 
    Article 

    Google Scholar 
    40.Williamson, D. H. et al. Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park. Mol. Ecol. 25, 6039–6054 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Almany, G. R. et al. Larval fish dispersal in a coral-reef seascape. Nat. Ecol. Evol. 1, 0148 (2017).Article 

    Google Scholar 
    42.Bode, M. et al. Successful validation of a larval dispersal model using genetic parentage data. PLOS Biol. 17, e3000380 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Nakae, M., Asaoka, R., Wada, H. & Sasaki, K. Fluorescent dye staining of neuromasts in live fishes: an aid to systematic studies. Ichthyol. Res. 59, 286–290 (2012).Article 

    Google Scholar 
    44.Webb, J. F. & Shirey, J. E. Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish. Dev. Dyn. 228, 370–385 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Becker, E. A., Bird, N. C. & Webb, J. F. Post-embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes. J. Morphol. 277, 1273–1291 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Webb, J. F. Morphological diversity, development, and evolution of the mechanosensory lateral line system. In The Lateral Line System (eds Coombs, S. et al.) 17–72 (Springer, 2014). https://doi.org/10.1007/2506_2013_12.Chapter 

    Google Scholar 
    47.Asaoka, R., Nakae, M. & Sasaki, K. The innervation and adaptive significance of extensively distributed neuromasts in Glossogobius olivaceus (Perciformes: Gobiidae). Ichthyol. Res. 59, 143–150 (2011).Article 

    Google Scholar 
    48.Asaoka, R., Nakae, M. & Sasaki, K. Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobioids (Perciformes: Rhyacichthyidae). Ichthyol. Res. 61, 49–58 (2014).Article 

    Google Scholar 
    49.Nickles, K. Ontogeny of the lateral line and visual systems of a Caribbean Reef Goby, Elacatinus lori (University of Rhode Island, 2019).50.Shand, J., Døving, K. B. & Collin, S. P. Optics of the developing fish eye: comparisons of Matthiessen’s ratio and the focal length of the lens in the black bream Acanthopagrus butcheri (Sparidae, Teleostei). Vis. Res. 39, 1071–1078 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Webb, J. F. et al. Development of the ear, hearing capabilities and laterophysic connection in the spotfin butterflyfish (Chaetodon ocellatus). Environ. Biol. Fishes 95, 275–290 (2012).Article 

    Google Scholar 
    52.Popper, A. N. & Hoxter, B. Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hear. Res. 15, 133–142 (1984).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Bever, M. M. & Fekete, D. M. Atlas of the developing inner ear in zebrafish. Dev. Dyn. 223, 536–543 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Haddon, C. & Lewis, J. Early ear development in the embryo of the Zebrafish, Danio rerio. J. Comp. Neurol. 365, 113–128 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Kawamura, G. et al. Morphogenesis of sense organs in the bluefin tuna Thunnus orientalis. in The Big Fish Bang Proceedings of the 26th Annual Larval Fish Conference (eds Browman, H. & Skiftesvik, A. B.) 123–135 (2003).
    Google Scholar 
    56.Pankhurst, P. M. & Butler, P. Development of the sensory organs in the greenback flounder, Rhombosolea tapirina. Mar. Freshw. Behav. Physiol. 28, 55–73 (1996).Article 

    Google Scholar 
    57.Lara, M. R. Morphology of the eye and visual acuities in the settlement-intervals of some Coral Reef Fishes (Labridae, Scaridae). Environ. Biol. Fishes 62, 365–378 (2001).Article 

    Google Scholar 
    58.Lara, M. R. Sensory Development in Settlement-Stage Larvae of Caribbean Labrids and Scarids: A Comparative Study with Implications for Ecomorphology and Life History Strategies (College of William and Mary, 1999).
    Google Scholar 
    59.Lecchini, D., Planes, S. & Galzin, R. Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav. Ecol. Sociobiol. 58, 18–26 (2005).Article 

    Google Scholar 
    60.Dixson, D. L. et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish. Oecologia 174, 99–107 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Irisson, J.-O., Guigand, C. & Paris, C. B. Detection and quantification of marine larvae orientation in the pelagic environment. Limnol. Oceanogr. Methods 7, 664–672 (2009).Article 

    Google Scholar 
    62.Irisson, J.-O., Paris, C. B., Leis, J. M. & Yerman, M. N. With a little help from my friends: group orientation by larvae of a coral reef fish. PLoS ONE 10, e0144060 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    63.Faillettaz, R., Blandin, A., Paris, C. B., Koubbi, P. & Irisson, J.-O. Sun-compass orientation in Mediterranean fish larvae. PLoS ONE 10, e0135213 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Lindo-Atichati, D., Curcic, M., Paris, C. B. & Buston, P. M. Description of surface transport in the region of the Belizean Barrier Reef based on observations and alternative high-resolution models. Ocean Model 106, 74–89 (2016).ADS 
    Article 

    Google Scholar 
    65.Agostinelli, C. & Lund, U. R package ‘circular’: Circular Statistics (version 0.4-93). https://r-forge.r-project.org/projects/circular/ (2017).66.R Core Team. R: A language and environment for statistical computing (R Found Stat Comput, 2013).
    Google Scholar 
    67.Leis, J., Hay, A. & Howarth, G. Ontogeny of in situ behaviours relevant to dispersal and population connectivity in larvae of coral-reef fishes. Mar. Ecol. Prog. Ser. 379, 163–179 (2009).ADS 
    Article 

    Google Scholar 
    68.Leis, J. M. & Carson-Ewart, B. M. (eds) The larvae of Indo-Pacific coastal fishes: an identification guide to marine fish larvae, 2nd edn. (Brill, 2004).
    Google Scholar 
    69.Kingsford, M. J. et al. Sensory environments, larval abilities and local self-recruitment. Bull. Mar. Sci. 70, 309–340 (2002).
    Google Scholar 
    70.Cresci, A. et al. Atlantic haddock (Melanogrammus aeglefinus) larvae have a magnetic compass that guides their orientation. iScience 19, 1173–1178 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl. Acad. Sci. 104, 858–863 (2007).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Dixson, D. L. et al. Coral reef fish smell leaves to find island homes. Proc. R. Soc. B Biol. Sci. 275, 2831–2839 (2008).Article 

    Google Scholar 
    73.Berenshtein, I. et al. Auto-correlated directional swimming can enhance settlement success and connectivity in fish larvae. J. Theor. Biol. 439, 76–85 (2018).MathSciNet 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Shaw, A. K., D’Aloia, C. C. & Buston, P. M. The evolution of marine larval dispersal kernels in spatially structured habitats: analytical models, individual-based simulations, and comparisons with empirical estimates. Am. Nat. 193, 424–435 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Ronce, O. & Clobert, J. Dispersal syndromes. In Dispersal Ecology and Evolution Vol. 55 (eds Clobert, J. et al.) 119–138 (Oxford University Press, Oxford, 2012).Chapter 

    Google Scholar 
    77.Huebert, K. & Sponaugle, S. Observed and simulated swimming trajectories of late-stage coral reef fish larvae off the Florida Keys. Aquat. Biol. 7, 207–216 (2009).Article 

    Google Scholar 
    78.Hamilton, W. D. & May, R. M. Dispersal in stable habitats. Nature 269, 578–581 (1977).ADS 
    Article 

    Google Scholar 
    79.Leis, J. et al. In situ orientation of fish larvae can vary among regions. Mar. Ecol. Prog. Ser. 537, 191–203 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    80.Botsford, L. W. et al. Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28, 327–337 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.White, J. W., Botsford, L. W., Hastings, A. & Largier, J. L. Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal. Mar. Ecol. Prog. Ser. 398, 49–67 (2010).ADS 
    Article 

    Google Scholar 
    82.Green, A. L. et al. Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design: connectivity and marine reserves. Biol. Rev. https://doi.org/10.1111/brv.12155 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    83.Munguia-Vega, A. et al. Ecological guidelines for designing networks of marine reserves in the unique biophysical environment of the Gulf of California. Rev. Fish Biol. Fish. 28, 749–776 (2018).Article 

    Google Scholar 
    84.Cowen, R. K., Paris, C. B. & Srinivasan, A. Scaling of connectivity in marine populations. Science 311, 522–527 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    85.Paris, C. B., Chérubin, L. M. & Cowen, R. K. Surfing, spinning, or diving from reef to reef: effects on population connectivity. Mar. Ecol. Prog. Ser. 347, 285–300 (2007).ADS 
    Article 

    Google Scholar 
    86.Mann, D. A., Casper, B. M., Boyle, K. S. & Tricas, T. C. On the attraction of larval fishes to reef sounds. Mar. Ecol. Prog. Ser. 338, 307–310 (2007).ADS 
    Article 

    Google Scholar 
    87.Esri. World Imagery [basemap]. 500m. Imagery, basemaps, and land cover. May 14, 2020. https://www.arcgis.com/home/webmap/viewer.html. (2020). More

  • in

    Short term fluctuating temperature alleviates Daphnia stoichiometric constraints

    1.Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article 

    Google Scholar 
    2.Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706. https://doi.org/10.1038/nature09407 (2010).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Elser, J. J. et al. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3, 540–550 (2000).Article 

    Google Scholar 
    4.Elser, J., Obrien, W., Dobberfuhl, D. & Dowling, T. The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J. Evol. Biol. 13, 845–853 (2000).Article 

    Google Scholar 
    5.Hessen, D. O., Elser, J. J., Sterner, R. W. & Urabe, J. Ecological stoichiometry: An elementary approach using basic principles. Limnol. Oceanogr. 58, 2219–2236 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    6.Hessen, D. O., Faerovig, P. J. & Andersen, T. Light, nutrients, and P : C ratios in algae: Grazer performance related to food quality and quantity. Ecology 83, 1886–1898 (2002).Article 

    Google Scholar 
    7.Moody, E. K., Rugenski, A. T., Sabo, J. L., Turner, B. L. & Elser, J. J. Does the growth rate hypothesis apply across temperatures? Variation in the growth rate and body phosphorus of neotropical benthic grazers. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2017.00014 (2017).Article 

    Google Scholar 
    8.Prater, C., Wagner, N. D. & Frost, P. C. Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations. Limnol. Oceanogr. 63, 1727–1740. https://doi.org/10.1002/lno.10803 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Boersma, M. et al. Temperature driven changes in the diet preference of omnivorous copepods: No more meat when it’s hot?. Ecol. Lett. 19, 45–53. https://doi.org/10.1111/ele.12541 (2016).Article 
    PubMed 

    Google Scholar 
    10.Wojewodzic, M. W., Kyle, M., Elser, J. J., Hessen, D. O. & Andersen, T. Joint effect of phosphorus limitation and temperature on alkaline phosphatase activity and somatic growth in Daphnia magna. Oecologia 165, 837–846. https://doi.org/10.1007/s00442-010-1863-2 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    11.Starke, C. W. E., Jones, C. L. C., Burr, W. S. & Frost, P. C. Interactive effects of water temperature and stoichiometric food quality on Daphnia pulicaria. Freshwat. Biol. 66, 256–265. https://doi.org/10.1111/fwb.13633 (2020).CAS 
    Article 

    Google Scholar 
    12.Ruiz, T. et al. U-shaped response Unifies views on temperature dependency of stoichiometric requirements. Ecol. Lett. 23, 860–869. https://doi.org/10.1111/ele.13493 (2020).Article 
    PubMed 

    Google Scholar 
    13.Persson, J., Wojewodzic, M. W., Hessen, D. O. & Andersen, T. Increased risk of phosphorus limitation at higher temperatures for Daphnia magna. Oecologia 165, 123–129. https://doi.org/10.1007/s00442-010-1756-4 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    14.Malzahn, A. M., Doerfler, D. & Boersma, M. Junk food gets healthier when it’s warm. Limnol. Oceanogr. 61, 1677–1685. https://doi.org/10.1002/lno.10330 (2016).ADS 
    Article 

    Google Scholar 
    15.Cross, W. F., Hood, J. M., Benstead, J. P., Huryn, A. D. & Nelson, D. Interactions between temperature and nutrients across levels of ecological organization. Glob. Change Biol. 21, 1025–1040. https://doi.org/10.1111/gcb.12809 (2015).ADS 
    Article 

    Google Scholar 
    16.Woods, H. A. et al. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17, 237–245. https://doi.org/10.1046/j.1365-2435.2003.00724.x (2003).Article 

    Google Scholar 
    17.Cotner, J. B., Makino, W. & Biddanda, B. A. Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26–33. https://doi.org/10.1007/s00248-006-9040-1 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Hessen, D. O. et al. Changes in stoichiometry, cellular RNA, and alkaline phosphatase activity of Chlamydomonas in response to temperature and nutrients. Front. Microbiol. 8, 18. https://doi.org/10.3389/fmicb.2017.00018 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Van Geest, G. J., Sachse, R., Brehm, M., van Donk, E. & Hessen, D. Maximizing growth rate at low temperatures: RNA:DNA allocation strategies and life history traits of Arctic and temperate Daphnia. Polar Biol. 33, 1255–1262 (2010).Article 

    Google Scholar 
    20.Prater, C., Wagner, N. D. & Frost, P. C. Interactive effects of genotype and food quality on consumer growth rate and elemental content. Ecology 98, 1399–1408. https://doi.org/10.1002/ecy.1795 (2017).Article 
    PubMed 

    Google Scholar 
    21.Lampert, W. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3, 21–27 (1989).Article 

    Google Scholar 
    22.Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P. & Breckenridge, J. K. Towards a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnol. Oceanogr. 56, 1603–1623 (2011).ADS 
    Article 

    Google Scholar 
    23.Dawidowicz, P. & Loose, C. J. Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol. Oceanogr. 37, 1589–1595 (1992).ADS 
    Article 

    Google Scholar 
    24.Mikulski, A., Grzesiuk, M., Rakowska, A., Bernatowicz, P. & Pijanowska, J. Thermal shock in Daphnia: cost of diel vertical migrations or inhabiting thermally-unstable waterbodies?. Fund. Appl. Limnol. 190, 213–220. https://doi.org/10.1127/fal/2017/0989 (2017).Article 

    Google Scholar 
    25.Reichwaldt, E. S., Wolf, I. D. & Stibor, H. Effects of a fluctuating temperature regime experienced by Daphnia during diel vertical migration on Daphnia life history parameters. Hydrobiologia 543, 199–205. https://doi.org/10.1007/s10750-004-7451-x (2005).Article 

    Google Scholar 
    26.Orcutt, J. D. & Porter, K. G. Diel vertical migration in zooplankton. Constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol. Oceanogr. 28, 720–730 (1983).ADS 
    Article 

    Google Scholar 
    27.Stich, H. B. & Lampert, W. Growth and reproduction of migrating and non-migrating Daphnia species under simulated food and temperature conditions of diurnal vertical migration. Oecologia 61, 192–196. https://doi.org/10.1007/BF00396759 (1984).ADS 
    Article 
    PubMed 

    Google Scholar 
    28.Fischer, J. M. et al. Diel vertical migration of copepods in mountain lakes: The changing role of ultraviolet radiation across a transparency gradient. Limnol. Oceanogr. 60, 252–262. https://doi.org/10.1002/lno.10019 (2015).ADS 
    Article 

    Google Scholar 
    29.Kessler, K., Lockwood, R. S., Williamson, C. E. & Saros, J. E. Vertical distribution of zooplankton in subalpine and alpine lakes: Ultraviolet radiation, fish predation, and the transparency-gradient hypothesis. Limnol. Oceanogr. 53, 2374–2382 (2008).ADS 
    Article 

    Google Scholar 
    30.Bergström, A.-K., Karlsson, J., Karlsson, D. & Vrede, T. Contrasting plankton stoichiometry and nutrient regeneration in northern arctic and boreal lakes. Aquat. Sci. https://doi.org/10.1007/s00027-018-0575-2 (2018).Article 

    Google Scholar 
    31.Sterner, R. W. On the phosphorus limitation paradigm for lakes. Int. Rev. Hydrobiol. 93, 433–445. https://doi.org/10.1002/iroh.200811068 (2008).CAS 
    Article 

    Google Scholar 
    32.Sterner, R. W. C: N: P stoichiometry in Lake superior: Freshwater sea as end member. Inland Waters 1, 29–46 (2011).CAS 
    Article 

    Google Scholar 
    33.Modenutti, B. E. et al. Environmental changes affecting light climate in oligotrophic mountain lakes: The deep chlorophyll maxima as a sensitive variable. Aquat. Sci. 75, 361–371. https://doi.org/10.1007/s00027-012-0282-3 (2013).CAS 
    Article 

    Google Scholar 
    34.Longhi, M. L. & Beisner, B. E. Environmental factors controlling the vertical distribution of phytoplankton in lakes. J. Plankton Res. 31, 1195–1207. https://doi.org/10.1093/plankt/fbp065 (2009).CAS 
    Article 

    Google Scholar 
    35.Leach, T. H. et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: The relative importance of light and thermal stratification. Limnol. Oceanogr. 63, 628–646. https://doi.org/10.1002/lno.10656 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Laspoumaderes, C. et al. Glacier melting and stoichiometric implications for lake community structure: Zooplankton species distributions across a natural light gradient. Glob. Change Biol. 19, 316–326. https://doi.org/10.1111/gcb.12040 (2013).ADS 
    Article 

    Google Scholar 
    37.Jacobs, A. F. G., Jetten, T. H., Lucassen, D., Heusinkveld, B. G. & Joost, P. N. Diurnal temperature fluctuations in a natural shallow water body. Agric. For. Meteorol. 88, 269–277. https://doi.org/10.1016/S0168-1923(97)00039-7 (1997).ADS 
    Article 

    Google Scholar 
    38.Vilas, M. P., Marti, C. L., Adams, M. P., Oldham, C. E. & Hipsey, M. R. Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: A proposed feedback mechanism of macrophyte loss. Front. Plant Sci. 8, 2097. https://doi.org/10.3389/fpls.2017.02097 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Burks, R. L., Lodge, D. M., Jeppesen, E. & Lauridsen, T. L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshwat. Biol. 47, 343–365 (2002).Article 

    Google Scholar 
    40.Morris, D. P. et al. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40, 1381–1391 (1995).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Balseiro, E. G., Modenutti, B. E., Queimaliños, C. & Reissig, M. Daphnia distribution in Andean Patagonian lakes: Effect of low food quality and fish predation. Aquat. Ecol. 41, 599–609 (2007).CAS 
    Article 

    Google Scholar 
    42.Modenutti, B. E., Wolinski, L., Souza, M. S. & Balseiro, E. G. When eating a prey is risky: Implications for predator diel vertical migration. Limnol. Oceanogr. 63, 939–950. https://doi.org/10.1002/lno.10681 (2018).ADS 
    Article 

    Google Scholar 
    43.Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73. https://doi.org/10.1038/417070a (2002).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Acharya, K., Kyle, M. & Elser, J. J. Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnol. Oceanogr. 49, 656–665 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Souza, M. S., Hansson, L.-A., Hylander, S., Modenutti, B. E. & Balseiro, E. G. Rapid enzymatic response to compensate UV radiation in copepods. PLoS ONE 7, e32046. https://doi.org/10.1371/journal.pone.0032046 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Wolinski, L., Modenutti, B., Souza, M. S. & Balseiro, E. Interactive effects of temperature, ultraviolet radiation and food quality on zooplankton alkaline phosphatase activity. Environ. Pollut. 213, 135–142. https://doi.org/10.1016/j.envpol.2016.02.016 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Xie, J. et al. Physiological effects of compensatory growth during the larval stage of the ladybird Cryptolaemus montrouzieri. J. Insect Physiol. 83, 37–42. https://doi.org/10.1016/j.jinsphys.2015.11.001 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Dmitriew, C. & Rowe, L. Resource limitation, predation risk and compensatory growth in a damselfly. Oecologia 142, 150–154. https://doi.org/10.1007/s00442-004-1712-2 (2005).ADS 
    Article 
    PubMed 

    Google Scholar 
    49.Malzahn, A. M. & Boersma, M. Effects of poor food quality on copepod growth are dose dependent and non-reversible. Oikos 121, 1408–1416. https://doi.org/10.1111/j.1600-0706.2011.20186.x (2012).Article 

    Google Scholar 
    50.Droop, M. R. Some thoughts on nutrient limitation in algae. J. PhycoI. 9, 264–272 (1973).CAS 
    Article 

    Google Scholar 
    51.Boersma, M. The nutritional quality of P-limited algae for Daphnia. Limnol. Oceanogr. 45, 1157–1161 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    52.Plath, K. & Boersma, M. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 82, 1260–1269 (2001).Article 

    Google Scholar 
    53.Barbiero, R. P. & Tuchman, M. L. Results from the US EPA’s biological open water surveillance program of the Laurentian Great Lakes: II. Deep chlorophyll maxima. J. Great Lakes Res. 27, 155–166 (2001).CAS 
    Article 

    Google Scholar 
    54.Camacho, A. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica 25, 453–478 (2006).
    Google Scholar 
    55.Pérez, G. L., Queimaliños, C. P. & Modenutti, B. E. Light climate and plankton in the deep chlorophyll maxima in North Patagonian Andean lakes. J. Plankton Res. 24, 591–599 (2002).Article 

    Google Scholar 
    56.Magee, M. R. & Wu, C. H. Response of water temperatures and stratification to changing climate in three lakes with different morphometry. Hydrol. Earth Syst. Sci. 21, 6253–6274. https://doi.org/10.5194/hess-21-6253-2017 (2017).ADS 
    Article 

    Google Scholar 
    57.Niedrist, G. H., Psenner, R. & Sommaruga, R. Climate warming increases vertical and seasonal water temperature differences and inter-annual variability in a mountain lake. Clim. Change 151, 473–490. https://doi.org/10.1007/s10584-018-2328-6 (2018).ADS 
    Article 

    Google Scholar 
    58.Kilham, S. S., Kreeger, D. A., Lynn, S. G., Goulden, C. E. & Herrera, L. COMBO – A defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377, 147–159 (1998).CAS 
    Article 

    Google Scholar 
    59.Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide c. J. Phycol. 8, 10–14 (1972).CAS 

    Google Scholar 
    60.Balseiro, E. G., Souza, M. S., Modenutti, B. E. & Reissig, M. Living in transparent lakes: Low food P: C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnol. Oceanogr. 53, 2383–2390 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    61.Laspoumaderes, C., Souza, M. S., Modenutti, B. E. & Balseiro, E. Glacier melting and response of Daphnia oxidative stress. J. Plankton Res. 39, 675–686. https://doi.org/10.1093/plankt/fbx028 (2017).CAS 
    Article 

    Google Scholar 
    62.APHA. Standard methods for the examination of water and wastewater. (American Public Health Association, AWWA, 2005).63.Gorokhova, E. & Kyle, M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J. Plankton Res. 24, 511–522 (2002).CAS 
    Article 

    Google Scholar  More

  • in

    The role of anthropogenic disturbance and invasion of yellow crazy ant in a recent decline of land crab population

    1.Holway, D. A., Lach, L., Suarez, A. V., Tsutsui, N. D. & Case, T. J. The cause and consequences of ant invasions. Annu. Rev. Ecol. Systemat. 33, 181–233 (2002).Article 

    Google Scholar 
    2.Moller, H. Lessons for invasion theory from social insects. Biol. Conserv. 78, 125–142 (1996).Article 

    Google Scholar 
    3.Hoffmann, B. D. & Saul, W. C. Yellow crazy ant (Anoplolepis gracilipes) invasions within undisturbed mainland Australian habitats: no support for biotic resistance hypothesis. Biol. Invasions 12, 3093–3108 (2010).Article 

    Google Scholar 
    4.Human, K. G. & Gordon, D. M. Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105, 405–412 (1996).ADS 
    PubMed 
    Article 

    Google Scholar 
    5.Walker, K. L. Impact of the little fire ant, Wasmannia auropunctata, on native forest ants in Gabon. Biotropica 38, 666–673 (2006).Article 

    Google Scholar 
    6.Cole, F. R., Medeiros, A. C., Loope, L. L. & Zuehlke, W. W. Effects of the Argentine ant on arthropod fauna of Hawaiian high-elevation shrubland. Ecology 73, 1313–1322 (1992).Article 

    Google Scholar 
    7.Porter, S. D. & Savignano, D. A. Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71, 2095–2106 (1990).Article 

    Google Scholar 
    8.Feare, C. Ants take over from rats on Bird Island, Seychelles. Bird Conserv. Int. 9, 95–96 (1999).Article 

    Google Scholar 
    9.Laakkonen, J., Fisher, R. N. & Case, T. J. Effect of land cover, habitat fragmentation, and ant colonies on the distribution and abundance of shrews in southern California. J. Anim. Ecol. 70, 776–788 (2001).Article 

    Google Scholar 
    10.Wojcik, D. P. et al. Red imported fire ants: impact on biodiversity. Am. Entomol. 47, 16–23 (2001).Article 

    Google Scholar 
    11.O’Dowd, D. J., Green, P. T. & Lake, P. S. Invasional ‘meltdown’ on an oceanic island. Ecol. Lett. 6, 812–817 (2003).Article 

    Google Scholar 
    12.Ness, J. H. & Bronstein, J. L. The effects of invasive ants on prospective ant mutualists. Biol. Invasions 6, 445–461 (2004).Article 

    Google Scholar 
    13.Buczkowski, G. & Bennett, G. Seasonal polydomy in a polygynous supercolony of the odorous house ant, Tapinoma sessile. Ecol. Entomol. 33, 780–788 (2008).
    Google Scholar 
    14.Menke, S. B., Fisher, R. N., Jetz, W. & Holway, D. A. Biotic and abiotic controls of Argentine ant invasion success at local and landscape scales. Ecology 88, 3164–3173 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Roura-Pascual, N. et al. Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader. Proc. Natl. Acad. Sci. USA 108, 220–225 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Bos, M. M., Tylianakis, J. M., Steffan-Dewenter, I. & Tsharntke, T. The invasive yellow crazy ant and the decline of forest ant diversity in Indonesian cacao agroforests. Biol. Invasions 10, 1399–1409 (2008).Article 

    Google Scholar 
    17.Human, K. G., Weiss, S., Weiss, A., Sandler, B. & Gordon, D. M. Effects of abiotic factors on the distribution and activity of the invasive Argentine ant (Hymenoptera: Formicidae). Environ. Entomol. 27, 822–833 (1998).Article 

    Google Scholar 
    18.Suarez, A. V., Holway, D. A. & Case, T. J. Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc. Natl. Acad. Sci. USA 98, 1095–1100 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Ito, F., Asfiya, W. & Kojima, J. I. Discovery of independent-founding solitary queens in the yellow crazy ant Anoplolepis gracilipes in East Java, Indonesia (Hymenoptera: Formicidae). Entomol. Sci. 19, 312–314 (2016).Article 

    Google Scholar 
    20.Lee, C. C., Lin, C. Y., Hsu, H. W. & Yang, C. C. S. Complete genome sequences of two novel dicistroviruses detected in yellow crazy ants (Anoplolepis gracilipes). Arch. Virol. 165, 2715–2719 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Wetterer, J. K. Worldwide distribution and potential spread of the long-legged ant, Anoplolepis gracilipes (Hymenoptera: Formicidae). Sociobiology 45, 77–97 (2005).
    Google Scholar 
    22.Abbott, K. L., Greaves, S. N. J., Ritchie, P. A. & Lester, P. J. Behaviourally and genetically distinct populations of an invasive ant provide insight into invasion history and impacts on a tropical ant community. Biol. Invasions 9, 453–463 (2007).Article 

    Google Scholar 
    23.Haines, I. H., Haines, J. B. & Cherrett, J. M. The impact and control of the crazy ant, Anoplolepis Longipes (Jerd.), in the Seychelles. In Exotic ants. Biology, impact and control of introduced species (ed. Williams, D. F.) 206–218 (Westview Press, 1994).
    Google Scholar 
    24.Gerlach, J. Impact of the invasive ant Anoplolepis gracilipes on Bird Island, Seychelles. J. Insect Conserv. 8, 15–25 (2004).Article 

    Google Scholar 
    25.Hill, M., Holm, K., Vel, T., Shah, N. J. & Matyot, P. Impact of the introduced yellow crazy ant Anoplolepis gracilipes on Bird Island, Seychelles. Biodivers. Conserv. 12, 1969–1984 (2003).Article 

    Google Scholar 
    26.Hoffmann, B. D., Auina, S. & Stanley, M. C. Targeted research to improve invasive species management: yellow crazy ant Anoplolepis gracilipes in Samoa. PLoS ONE 9, e95301 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Kaiser-Bunbury, C. N., Cuthbert, H., Fox, R., Birch, D. & Bunburry, N. Invasion of yellow crazy ant Anoplolepis gracilipes in a Seychelles UNESCO palm forest. NeoBiota 22, 43–57 (2014).Article 

    Google Scholar 
    28.Wheeler, W. M. Ants of Formosa and the Philippines. Bull. Am. Mus. Nat. Hist. 26, 333–345 (1909).
    Google Scholar 
    29.Hsu, P. C. The study of habitats distribution of exotic invasive ants in Taiwan by using bait traps. Master dissertation, National Changhua University of Education (2013) (In Chinese).30.Tseng, H. H. The ant community structure at Kenting National Park in Taiwan. Master dissertation, National Changhua University of Education (2013) (In Chinese).31.Hsu, J. W. & Shih, H. T. Diversity of Taiwanese Brackish crabs genus Ptychognathus Stimpson, 1858 (Crustacea: Brachyura: Varunidae) based on DNA barcodes, with descriptions of two new species. Zool. Stud. 59, 59 (2020).CAS 

    Google Scholar 
    32.Li, J. J., Shih, H. T. & Ng, P. K. Three new species and two new records of Parasesarma De Man, 1895 (Crustacea: Brachyura: Sesarmidae) from Taiwan and the Philippines from morphological and molecular evidence. Zool. Stud. 58, 40 (2019).CAS 

    Google Scholar 
    33.Li, J. J., Hsu, J. W., Ng, N. K. & Shih, H. T. Eight new records of crabs (Decapoda, Brachyura: Sesarmidae, Varunidae) from the coasts of Taiwan. Crustaceana 92, 1207–1230 (2019).Article 

    Google Scholar 
    34.Li, J. J., Shih, H. T. & Ng, P. K. The Taiwanese and Philippine species of the terrestrial crabs Bresedium Serène and Soh, 1970 and Sesarmops Serène and Soh, 1970 (Crustacea: Decapoda: Brachyura), with descriptions of two new species. Zool. Stud. 59, 16 (2020).CAS 

    Google Scholar 
    35.Liu, H. C. Report on the survey of ecological resources of land crab in Kenting National Park 2019–2020. Consultancy Report to Kenting National Park Headquarters, p. 155 (2020) (In Chinese).36.Ng, P. K., Li, J. J. & Shih, H. T. What is Sesarmops impressus (H. Milne Edwards, 1837) (Crustacea: Brachyura: Sesarmidae)?. Zool. Stud. 59, 27 (2020).CAS 

    Google Scholar 
    37.Shih, H. T., Hsu, J. W., Li, J. J., Ng, N. K. & Lee, J. H. The identities of three species of Parahelice Sakai, Türkay & Yang, 2006 (Crustacea: Brachyura: Varunidae) from the western Pacific, based on morphological and molecular evidence. Zootaxa 4728, 249–265 (2020).Article 

    Google Scholar 
    38.Liu, H. C. Biodiversity and population abundance of the land crab fauna both at Houwan and Hsiangchiaowan-Shadao areas of the Kenting National Park. Consultancy Report to Kenting National Park Headquarters, p. 102 (2016) (In Chinese)39.Lin, C. C., Chang, T. W., Chen, H. W., Shih, C. H. & Hsu, P. C. Development of liquid bait with unique bait station for control of Dolichoderus thoracicus (Hymenoptera: Formicidae). J. Econ. Entomol. 110, 1685–1692 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    40.Haines, I. H. & Haines, J. B. Colony structure, seasonality and food requirements of the crazy ant, Anoplolepis longipes (Jerd.), in the Seychelles. Ecol. Entomol. 3, 109–118 (1978).Article 

    Google Scholar 
    41.Ho, P. H. Land crabs at coastal forests in Kenting National Park, p. 47 (Kenting National Park Headquarters, 2003) (In Chinese).42.Tung, G. S., Chang, T. P. & Liu, H. C. Monitor and comparison of terrestrial crab communities in the virgin and restoration tropical coastal forests in Kenting National Park. J. Natl. Park 23, 21–30 (2013).
    Google Scholar 
    43.National Land Survey and Mapping Center (NLSC). The Second National Land-Use Survey (Ministry of Interior, 2008).44.ESRI. ArcGIS Desktop: Release 10 (Environmental Systems Research Institute, 2011).45.R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018. Available online: https://www.R-project.org/, accessed 20 December 2018.46.Lester, P. J. & Tavite, A. Long-legged ants, Anoplolepis gracilipes (Hymenoptera: Formicidae), have invaded Tokelau, changing composition and dynamics of ant and invertebrate communities. Pac. Sci. 58, 391–401 (2004).Article 

    Google Scholar 
    47.Liu, H. C. & Jeng, M. S. Some reproductive aspects of Gecarcoidea lalandii (Brachyura: Gecarcinidae) in Taiwan. Zool. Stud. 46, 347–354 (2007).
    Google Scholar 
    48.Su, C. Y., Li, J. J., Wu, H. J. & Chiu, Y. W. An investigation of diversity and reproduction of land crab fauna in Houwan. J. Natl. Park 26, 49–57 (2014).
    Google Scholar 
    49.Baumgartner, N. R. II. & Ryan, S. D. Interaction of red crabs with yellow crazy ants during migration on Christmas Island. Math. Biosci. 330, 108486 (2020).MathSciNet 
    PubMed 
    MATH 
    Article 

    Google Scholar 
    50.Hicks, J. W. The breeding behaviour and migrations of the terrestrial crab Gecarcoidea natalis (Decapoda: Brachyura). Aust. J. Zool. 33, 127–142 (1985).Article 

    Google Scholar 
    51.Green, P. T., O’Dowd, D. J. & Lake, P. S. Alien ant invasion and ecosystem collapse on Christmas Island, Indian Ocean. Aliens 9, 2–4 (1999).
    Google Scholar 
    52.Li, J. J. & Chiu, Y. W. An atlas of land crabs on Hengchun Peninsula 2.0, p. 136 (National Museum of Marine Biology and Aquarium, 2019) (In Chinese).53.Liu, H. C. Land crab resource survey and management plan in Kenting National Park. Consultancy Report to Kenting National Park Headquarters, p. 88 (2010) (In Chinese).54.Achury, R., Chacón de Ulloa, P., Arcila, Á. & Suarez, A. V. Habitat disturbance modifies dominance, coexistence, and competitive interactions in tropical ant communities. Ecol. Entomol. 45, 1247–1262 (2020).Article 

    Google Scholar 
    55.Lessard, J. P. & Buddle, C. M. The effects of urbanization on ant assemblages (Hymenoptera: Formicidae) associated with the Molson Nature Reserve, Quebec. Can. Entomol. 137, 215–225 (2005).Article 

    Google Scholar 
    56.Mauda, E. V., Joseph, G. S., Seymour, C. L., Munyai, T. C. & Foord, S. H. Changes in landuse alter ant diversity, assemblage composition and dominant functional groups in African savannas. Biodivers. Conserv. 27, 947–965 (2018).Article 

    Google Scholar 
    57.Bacon, S. J., Aebi, A., Calanca, P. & Bacher, S. Quarantine arthropod invasions in Europe: the role of climate, hosts and propagule pressure. Divers. Distrib. 20, 84–94 (2014).Article 

    Google Scholar 
    58.Tschinkel, W. R. Distribution of the fire ants Solenopsis invicta and S. geminata (Hymenoptera: Formicidae) in Northern Florida in relation to habitat and disturbance. Ann. Entomol. Soc. Am. 81, 76–81 (1988).Article 

    Google Scholar 
    59.Pyšek, P. et al. Disentangling the role of environmental and human pressure on biological invasions across Europe. Proc. Natl. Acad. Sci. USA 107, 12157–12162 (2010).ADS 
    PubMed 
    Article 

    Google Scholar 
    60.Rizali, A. et al. Ant communities on small tropical islands: effects of island size and isolation are obscured by habitat disturbance and ‘tramp’ ant species. J. Biogeogr. 37, 229–236 (2010).Article 

    Google Scholar 
    61.Rao, N. S., Veeresh, G. K. & Viraktamath, C. A. Dispersal and spread of crazy ant Anoplolepis longipes (Jerdon)(Hymenoptera: Formicidae). Environ. Ecol. 9, 682–686 (1991).
    Google Scholar 
    62.Gordon, D. M., Moses, L., Falkovitz-Halpern, M. & Wong, E. H. Effect of weather on infestation of buildings by the invasive Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Am. Midl. Nat. 146, 321–328 (2001).Article 

    Google Scholar 
    63.Menke, S. B. & Holway, D. A. Abiotic factors control invasion by Argentine ants at the community scale. J. Anim. Ecol 75, 368–376 (2006).PubMed 
    Article 

    Google Scholar 
    64.Hsu, P. W. et al. Ant crickets (Orthoptera: Myrmecophilidae) associated with the invasive yellow crazy ant Anoplolepis gracilipes (Hymenoptera: Formicidae): evidence for cryptic species and potential co-introduction with hosts. Myrmecol. News 30, 103–129 (2020).
    Google Scholar 
    65.Rao, N. S. & Veeresh, G. K. Nesting and foraging habits of crazy ant Anoplolepis longipes (Jerdon) (Hymenoptera: Formicidae). Environ. Ecol. 9, 670–677 (1991).
    Google Scholar 
    66.Vonshak, M. & Gordon, D. M. Intermediate disturbance promotes invasive ant abundance. Biol. Conserv. 186, 359–367 (2015).Article 

    Google Scholar 
    67.Yodzis, P. How rare is omnivory?. Ecology 65, 321–323 (1984).Article 

    Google Scholar 
    68.Linquist, E. S. et al. Land crabs as key drivers in tropical coastal forest recruitment. Biol. Rev. 84, 203–223 (2009).Article 

    Google Scholar 
    69.Koch, V. & Wolff, M. Energy budget and ecological role of mangrove epibenthos in the Caeté estuary, North Brazil. Mar. Ecol. Prog. Ser. 228, 119–130 (2002).ADS 
    Article 

    Google Scholar  More

  • in

    Polymetallic nodules are essential for food-web integrity of a prospective deep-seabed mining area in Pacific abyssal plains

    1.Ramírez-Llodrà, E. et al. Man and the last great wilderness: Human impact on the deep sea. PLoS ONE 6, e22588 (2011).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    2.Hein, J. R. & Koschinsky, A. Deep-ocean ferromanganese crusts and nodules. in Treatise on Geochemistry (eds. Holland, H. & Turekian, K.) vol. 13 273–291 (Elsevier Ltd., 2014).3.Hein, J. R. Manganese nodules. Encyclop. Mar. Geosci. 1, 408–412 (2016).
    Google Scholar 
    4.Kuhn, T., Wegorzewski, A. V., Rühlemann, C. & Vink, A. Composition, formation, and occurrence of polymetallic nodules. in Deep-Sea Mining (ed. Sharma, R.) 23–63 (Springer International Publishing, 2017). https://doi.org/10.1007/978-3-319-52557-0_2.5.Amon, D. J. et al. Insights into the abundance and diversity of abyssal megafauna in a polymetallic-nodule region in the eastern Clarion–Clipperton Zone. Sci. Rep. 6, 1–12 (2016).Article 
    CAS 

    Google Scholar 
    6.Purser, A. et al. Association of deep-sea incirrate octopods with manganese crusts and nodule fields in the Pacific Ocean. Curr. Biol. 26, R1268–R1269 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Vanreusel, A., Hilário, A., Ribeiro, P. A., Menot, L. & Martínez Arbizu, P. Threatened by mining, polymetallic nodules are required to preserve abyssal epifauna. Sci. Rep. 6, 26808 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Iken, K., Brey, T., Wand, U., Voigt, J. & Junghans, P. Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): A stable isotope analysis. Prog. Oceanogr. 50, 383–405 (2001).ADS 
    Article 

    Google Scholar 
    9.Aberle, N. & Witte, U. Deep-sea macrofauna exposed to a simulated sedimentation event in the abyssal NE Atlantic: In situ pulse-chase experiments using 13C-labelled phytodetritus. Mar. Ecol. Prog. Ser. 251, 37–47 (2003).ADS 
    Article 

    Google Scholar 
    10.Sweetman, A. K. & Witte, U. Response of an abyssal macrofaunal community to a phytodetrital pulse. Mar. Ecol. Prog. Ser. 355, 73–84 (2008).ADS 
    Article 

    Google Scholar 
    11.van Oevelen, D., Soetaert, K. & Heip, C. H. R. Carbon flows in the benthic food web of the Porcupine Abyssal Plain: The (un)importance of labile detritus in supporting microbial and faunal carbon demands. Limnol. Oceanogr. 57, 645–664 (2012).ADS 
    Article 
    CAS 

    Google Scholar 
    12.Dunlop, K. M. et al. Carbon cycling in the deep eastern North Pacific benthic food web: Investigating the effect of organic carbon input. Limnol. Oceanogr. 61, 1956–1968 (2016).ADS 
    Article 

    Google Scholar 
    13.de Jonge, D. S. W. et al. Abyssal food-web model indicates faunal carbon flow recovery and impaired microbial loop 26 years after a sediment disturbance experiment. Prog. Oceanogr. 189, 102446 (2020).Article 

    Google Scholar 
    14.Smith, C. R., De Léo, F. C., Bernardino, A. F., Sweetman, A. K. & Martínez Arbizu, P. Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23, 518–528 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Meysman, F. J. R., Middelburg, J. J. & Heip, C. H. R. Bioturbation: A fresh look at Darwin’s last idea. Trends Ecol. Evol. 21, 688–695 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.van der Zee, E. M. et al. How habitat-modifying organisms structure the food web of two coastal ecosystems. Proc. R. Soc. B Biol. Sci. 283, 20152326 (2016).Article 
    CAS 

    Google Scholar 
    17.Giere, O. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediment (Springer, 2009).
    Google Scholar 
    18.Hall, S. J. & Raffaelli, D. G. Food webs: Theory and reality. Adv. Ecol. Res. 24, 187–239 (1993).Article 

    Google Scholar 
    19.Mahatma, R. Meiofauna communities of the Pacific nodule province: Abundance, diversity and community structure. PhD-Thesis (Carl von Ossietzky Universität Oldenburg, 2009).20.McIntyre, A. Ecoloy of marine meiobenthos. Biol. Rev. 44, 245–288 (1969).Article 

    Google Scholar 
    21.Borowski, C. Physically disturbed deep-sea macrofauna in the Peru Basin, Southeast Pacific, revisited 7 years after the experimental impact. Deep. Res. II(48), 3809–3839 (2001).ADS 

    Google Scholar 
    22.Kéfi, S. et al. More than a meal… integrating non-feeding interactions into food webs. Ecol. Lett. 15, 291–300 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Roberts, D. & Moore, H. M. Tentacular diversity in deep-sea deposit-feeding holothurians: Implications for biodiversity in the deep sea. Biodivers. Conserv. 6, 1487–1505 (1997).Article 

    Google Scholar 
    24.Buhl-Mortensen, L. et al. Habitat complexity and bottom fauna composition at different scales on the continental shelf and slope of northern Norway. Hydrobiologia 685, 191–219 (2012).Article 

    Google Scholar 
    25.Simon-Lledó, E. et al. Ecology of a polymetallic nodule occurrence gradient: Implications for deep-sea mining. Limnol. Oceanogr. 64, 1883–1894 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Hasemann, C. et al. Effects of dropstone-induced habitat heterogeneity on Arctic deep-sea benthos with special reference to nematode communities. Mar. Biol. Res. 9, 229–245 (2013).Article 

    Google Scholar 
    27.Riehl, T., Wölfl, A. C., Augustin, N., Devey, C. W. & Brandt, A. Discovery of widely available abyssal rock patches reveals overlooked habitat type and prompts rethinking deep-sea biodiversity. Proc. Natl. Acad. Sci. USA. 117, 15450–15459 (2020).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Kidd, R. B., Huggett, J. & Huggett, Q. J. Rock debris on abyssal plains in the northeast Atlantic: A comparison of epibenthic sledge hauls and photographic surveys. Oceanol. Acta 4, 99–104 (1981).
    Google Scholar 
    29.Gooday, A. J., Goineau, A. & Voltski, I. Abyssal foraminifera attached to polymetallic nodules from the eastern Clarion-Clipperton Fracture Zone: A preliminary description and comparison with North Atlantic dropstone assemblages. Mar. Biodivers. 45, 391–412 (2015).Article 

    Google Scholar 
    30.Ziegler, A. F., Smith, C. R., Edwards, K. F. & Vernet, M. Glacial dropstones: Islands enhancing seafloor species richness of benthic megafauna in West Antarctic Peninsula fjords. Mar. Ecol. Prog. Ser. 583, 1–14 (2017).ADS 
    Article 

    Google Scholar 
    31.Schulz, M., Bergmann, M., von Juterzenka, K. & Soltwedel, T. Colonisation of hard substrata along a channel system in the deep Greenland Sea. Polar Biol. 33, 1359–1369 (2010).Article 

    Google Scholar 
    32.Simon-Lledó, E. et al. Multi-scale variations in invertebrate and fish megafauna in the mid-eastern Clarion Clipperton Zone. Prog. Oceanogr. 187, 102405 (2020).Article 

    Google Scholar 
    33.Ilan, M., Ben-Eliahu, M. N. & Galil, B. Three deep water sponges from the eastern Mediterranean and their associated Fauna. Ophelia 39, 45–54 (1994).Article 

    Google Scholar 
    34.Beaulieu, S. E. Colonization of habitat islands in the deep sea: Recruitment to glass sponge stalks. Deep. Res. I(48), 1121–1137 (2001).Article 

    Google Scholar 
    35.Buhl-Mortensen, L. et al. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar. Ecol. 31, 21–50 (2010).ADS 
    Article 

    Google Scholar 
    36.Huston, M. A. Introduction. in Biological Diversity. The coexistence of species on changing landscapes 1–11 (Cambridge University Press, 1994).37.Beaulieu, S. E. Life on glass houses: Sponge stalk communities in the deep sea. Mar. Biol. 138, 803–817 (2001).Article 

    Google Scholar 
    38.Dunne, J. A., Williams, R. J. & Martinez, N. D. Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5, 558–567 (2002).Article 

    Google Scholar 
    39.Sole, R. V. & Montoya, M. Complexity and fragility in ecological networks. Proc. R. Soc. B Biol. Sci. 268, 2039–2045 (2001).CAS 
    Article 

    Google Scholar 
    40.Warren, P. H. Spatial and temporal variation in the structure of a freshwater food web. Oikos 55, 299–311 (1989).Article 

    Google Scholar 
    41.Van Dover, C. L. et al. Biodiversity loss from deep-sea mining. Nat. Geosci. 10, 464–465 (2017).ADS 
    Article 
    CAS 

    Google Scholar 
    42.Niner, H. J. et al. Deep-sea mining with no net loss of biodiversity: An impossible aim. Front. Mar. Sci. 5, 00195 (2018).Article 

    Google Scholar 
    43.Washburn, T. W. et al. Ecological risk assessment for deep-sea mining. Ocean Coast. Manag. 176, 24–39 (2019).Article 

    Google Scholar 
    44.Christodoulou, M. et al. Unexpected high abyssal ophiuroid diversity in polymetallic nodule fields of the northeast Pacific Ocean and implications for conservation. Biogeosciences 17, 1845–1876 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Christodoulou, M., O’Hara, T. D., Hugall, A. F. & Arbizu, P. M. Dark ophiuroid biodiversity in a prospective abyssal mine field. Curr. Biol. 29, 3909-3912.e3 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Ramírez-Llodrà, E. et al. Deep, diverse and definitely different: Unique attributes of the world’s largest ecosystem. Biogeosciences 7, 2851–2899 (2010).ADS 
    Article 

    Google Scholar 
    47.International Seabed Authority. Regulations on prospecting and exploration for polymetallic nodules in the Area. (2000).48.Stratmann, T. et al. Abyssal plain faunal carbon flows remain depressed 26 years after a simulated deep-sea mining disturbance. Biogeosciences 15, 4131–4145 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    49.Soetaert, K. & van Oevelen, D. Modeling food web interactions in benthic deep-sea ecosystems: A practical guide. Oceanography 22, 128–143 (2009).Article 

    Google Scholar 
    50.van Oevelen, D. et al. Quantifying food web flows using linear inverse models. Ecosystems 13, 32–45 (2010).Article 

    Google Scholar 
    51.International Seabed Authority. Draft environmental management plan for the Clarion-Clipperton Zone I. 1–18 (International Seabed Authority, 2011).52.Jung, H.-S., Lee, C.-B., Jeong, K.-S. & Kang, J.-K. Geochemical and mineralogical characteristics in two-color core sediments from the Korea Deep Ocean Study (KODOS) area, northeast equatorial Pacific. Mar. Geol. 144, 295–309 (1998).ADS 
    CAS 
    Article 

    Google Scholar 
    53.Wedding, L. M. et al. From principles to practice: A spatial approach to systematic conservation planning in the deep sea. Proc. R. Soc. B Biol. Sci. 280, 20131684 (2013).CAS 
    Article 

    Google Scholar 
    54.Hannides, A. K. & Smith, C. R. The Northeast Pacific abyssal plain. in Biogeochemistry of Marine Systems (eds. Black, K. D. & Shimmield, G. B.) 208–237 (Blackwell Publishing, 2003).55.International Seabed Authority. A geological model of polymetallic nodule deposits in the Clarion Clipperton Fracture Zone. ISA technical study No. 6. (2010).56.Schoening, T., Jones, D. O. B. & Greinert, J. Compact-morphology-based polymetallic nodule delineation. Sci. Rep. 7, 13338 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    57.Anonymous. Google Earth. https://www.google.com/earth/ (2018).58.Klein, H. Near-bottom currents in the deep Peru Basin, DISCOL experimental area. Dtsch. Hydrogr. Z. 45, 31–42 (1993).Article 

    Google Scholar 
    59.Bharatdwaj, K. Reliefs of the ocean basins. in Physical Geography (Oceanography) 1–53 (Discovery Publishing House, 2006).60.Glasby, G. P. Manganese: Predominant role of nodules and crusts. in Marine Geochemistry (eds. Schulz, H. D. & Zabel, M.) 371–427 (Springer-Verlag, 2006). https://doi.org/10.1007/3-540-32144-6_11.61.Haeckel, M., König, I., Riech, V., Weber, M. E. & Suess, E. Pore water profiles and numerical modelling of biogeochemical processes in Peru Basin deep-sea sediments. Deep. Res. I(48), 3713–3736 (2001).ADS 

    Google Scholar 
    62.Moher, D., Liberati, A., Tetzlaff, J. & Altman, D. G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 6, e1000097 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    63.Thiel, H. Use and protection of the deep sea: An introduction. Deep. Res. II(48), 3427–3431 (2001).ADS 

    Google Scholar 
    64.Anthropogenic disturbances in the deep sea. (Frontiers Media SA, 2019). https://doi.org/10.3389/978-2-88963-288-6.65.Assessing environmental impacts of deep-sea mining – revisiting decade-old benthic disturbances in Pacific nodule areas. Biogeosciences (2018).66.Martínez Arbizu, P. & Haeckel, M. RV SONNE Fahrtbericht/Cruise Report SO239. EcoResponse assessing the ecology, connectivity and resilience of polymetallic nodule field systems. vol. 25 (2015).67.Boetius, A. RV SONNE SO242/2. Cruise Report/Fahrtbericht. DISCOL revisited. Guayaquil: 28 August 2015: Guayaquil: 1 October 2015. SO242/2: JPI Oceans Ecological Aspects of Deep-Sea Mining. (2015).68.Horton, T. et al. World Register of Marine Species (WoRMS). http://www.marinespecies.org (2018). https://doi.org/10.14284/170.69.Ahnert, A. & Schriever, G. Response of abyssal copepoda Harpacticoida (Crustacea) and other meiobenthos to an artificial disturbance and its bearing on future mining for polymetallic nodules. Deep. Res. II 48, 3779–3794 (2001).ADS 
    CAS 
    Article 

    Google Scholar 
    70.Radziejewska, T. Responses of deep-sea meiobenthic communities to sediment disturbance simulating effects of polymetallic nodule mining. Int. Rev. Hydrobiol. 87, 457–477 (2002).Article 

    Google Scholar 
    71.Borowski, C. & Thiel, H. Deep-sea macrofaunal impacts of a large-scale physical disturbance experiment in the Southeast Pacific. Deep. Res. II 45, 55–81 (1998).ADS 
    Article 

    Google Scholar 
    72.Pimm, S. L., Lawton, J. H. & Cohen, J. E. Food web patterns and their consequences. Nature 350, 669–674 (1991).ADS 
    Article 

    Google Scholar  More

  • in

    Mangrove selective logging sustains biomass carbon recovery, soil carbon, and sediment

    Our analysis suggests that, over 465 ha of mangrove area, almost 83% of aboveground tree biomass were harvested annually for commercial timber purposes, using a keyhole harvest pattern (Fig. S3b). Yet after 25 years of natural and human-induced regeneration, both field- and satellite-based assessments reveal that biomass carbon stocks and canopy cover had fully recovered. Our approach using space-for-time substitution indicates that manual selective logging did not significantly affect soil carbon stocks and rates of annual carbon burial. While the differences in soil carbon stock between sites may be due to the diverse hydro-geomorphic settings8,14 the mangrove root mass in the top 1-m were not disturbed by manual logging activities. Similar situation was found in Tampa Bay, Florida where peat formation from root mass has enhance carbon sequestration15. These findings reduce uncertainty around the effects of mangrove forest management on the long-term functional capacity of blue carbon storage and provide evidence that managed mangrove ecosystems may deliver nature-based climate solutions.Recovery of forest structure, canopy cover and species diversityAlong carbon stocks, forest structure and species diversity also demonstrated recovery (Fig. 2, Table S1). Seedling densities were significantly higher in 5 year-old mangrove plots than in plots at any other stage (F(5,13) = 28.321, p  More