Multi-scale temporal variation of marine femtoplankton and picophytoplankton: the role of size and environment
DOI:
https://doi.org/10.1590/Keywords:
Flow cytometry, Time series, Generalized additive model, Upwelling, Virus-like particlesAbstract
Femtoplankton and picophytoplankton organisms exert a major role in the balance between producers and consumers and are responsible for a large part of net primary production in the ocean. However, despite their ecological importance, the magnitude and drivers of their temporal dynamics remain largely unexplored. To address this significant knowledge gap, we performed weekly sampling over ten months in a wind-driven coastal upwelling area in the subtropical South Atlantic Ocean. We combined this intensive feldwork with multi-color fow cytometry and statistical modeling to investigate the temporal changes of both femto- and picophytoplankton at multiple temporal scales. We found that femtoplanktonic organisms (including virus-like particles) responded faster (i.e., without a temporal lag) to environmental changes, mainly related to chlorophyll-a (chl-a) and phaeopigment variations. On the other hand, picophytoplanktonic organisms showed a slower response to environmental changes, with positive responses to variation in pH and NH4 concentrations after a one-week lag. Overall, our results demonstrate that the speed of response of planktonic organisms to environmental changes may be dependent on their size, which highlights the importance of environmental variables and biological interactions as drivers of their temporal dynamics.
References
AL-OTAIBI, N., HUETE-STAUFFER, T. M., CALLEJA, M. L., IRIGOIEN, X. & MORÁN, X. A. G. 2020. Seasonal variability and vertical distribution of autotrophic and heterotrophic picoplankton in the Central Red Sea. PeerJ, 8(2), e8612, DOI: https://doi.org/10.7717/peerj.8612
» https://doi.org/10.7717/peerj.8612
ANDERSEN, K. H., BERGE, T., GONÇALVES, R. J., HARTVIG, M., HEUSCHELE, J., HYLANDER, S., JACOBSEN, N. S., LINDEMANN, C., MARTENS, E. A., NEUHEIMER, A. B., OLSSON, K., PALACZ, A., PROWE, A. E. F., SAINMONT, J., TRAVING, S. J., VISSER, A. W., WADHWA, N. & KIORBOE, T. 2016. Characteristic sizes of life in the oceans, from bacteria to whales. Annual Review of Marine Science, 8, 217-241. DOI: https://doi.org/10.1146/annurev-marine-122414-034144
» https://doi.org/10.1146/annurev-marine-122414-034144
AZAM, F., FENCHEL, T., FIELD, J. G., GRAY, J. S., MEYER-REIL, L. A. & THINGSTAD, F. 1983. The ecological role of water column microbes in the sea. Marine Ecology Progress Series, 10, 257-263, DOI: https://doi.org/10.3354/meps010257
» https://doi.org/10.3354/meps010257
AZAM, F. & MALFATTI, F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10), 782-791, DOI: https://doi.org/10.1038/nrmicro1747
» https://doi.org/10.1038/nrmicro1747
BERGO, N. M., SIGNORI, C. N., AMADO, A. M., BRANDINI, F. P. & PELLIZARI, V. H. 2017. The partitioning of carbon biomass among the pico-and nano-plankton community in the South Brazilian bight during a strong summer intrusion of south Atlantic central water. Frontiers in Marine Science, 4, 1-12, DOI: https://doi.org/10.3389/fmars.2017.00238
» https://doi.org/10.3389/fmars.2017.00238
BOLAÑOS, L. M., CHANG, L. K., CHOI, J., WORDEN, A. Z., GRAFF, J. R., HAËNTJENS, N., CHASE, A. P., DELLA, A., GAUBE, P., MORISON, F., TOBY, S. M., ROBERT, K. W., EMMANUEL, T. O. M., MICHAEL, B. & GIOVANNONI, S. J. 2020. Small phytoplankton dominate western North Atlantic biomass. The ISME Journal, 14, 1663-1674, DOI: https://doi.org/10.1038/s41396-020-0636-0
» https://doi.org/10.1038/s41396-020-0636-0
BRAAK, C. J. F. & VAN DAME, H. 1989. Inferring pH from diatoms: a comparison of old and new calibration methods. Hydrobiologia, 178(3), 209-223, DOI: https://doi.org/10.1007/BF00006028
» https://doi.org/10.1007/BF00006028
BRUSSAARD, C. P. D. 2004. Optimization of procedures for counting viruses by fow cytometry. Applied and Environmental Microbiology, 70(3), 1506-1513, DOI: https://doi.org/10.1128/AEM.70.3.1506-1513.2004
» https://doi.org/10.1128/AEM.70.3.1506-1513.2004
CAMPOS, P. C., MÖLLER JUNIOR, O. O., PIOLA, A. R. & PALMA, E. D. 2013. Seasonal variability and coastal upwelling near Cape Santa Marta (Brazil). Journal of Geophysical Research: Oceans, 118(3), 1420-1433, DOI: https://doi.org/10.1002/jgrc.20131
» https://doi.org/10.1002/jgrc.20131
CASTELAO, R. M. & BARTH, J. A. 2006. Upwelling around Cabo Frio, Brazil: the importance of wind stress curl. Geophysical Research Letters, 33(3), 2-5, DOI: https://doi.org/10.1029/2005GL025182
» https://doi.org/10.1029/2005GL025182
CHAFFRON, S., DELAGE, E., BUDINICH, M., VINTACHE, D., HENRY, N., NEF, C., ARDYNA, M., ZAYED, A., JUNGER, P., GALAND, P., LOVEJOY, C., MURRAY, A., SARMENTO, H., OCEANS COORDINATORS, T., ACINAS, S., BABIN, M., IUDICONE, D., JAILLON, O., KARSENTI, E., WINCKER, P., KARP-BOSS, L., SULLIVAN, M., BOWLER, C., VARGAS, C. & EVEILLARD, D. 2020. Environmental vulnerability of the global ocean plankton community interactome. BioRxiv, 2020 Nov 10, [Epub preprint], DOI: https://doi.org/10.1101/2020.11.09.375295
» https://doi.org/10.1101/2020.11.09.375295
CHEN, C. Y. & DURBIN, E. G. 1994. Effects of pH on the growth and carbon uptake of marine phytoplankton. Marine Ecology Progress Series, 109(1), 83-94, DOI: https://doi.org/10.3354/meps109083
» https://doi.org/10.3354/meps109083
CLOERN, J. E. & JASSBY, A. D. 2010. Patterns and scales of phytoplankton variability in estuarine-coastal ecosystems. Estuaries and Coasts, 33(2), 230-241, DOI: https://doi.org/10.1007/s12237-009-9195-3
» https://doi.org/10.1007/s12237-009-9195-3
COELHO-SOUZA, S. A., LÓPEZ, M. S., GUIMARÃES, J. R. D., COUTINHO, R. & CANDELLA, R. N. 2012. Biophysical interactions in the Cabo Frio upwelling systems Southeastern Brazil. Brazilian Journal of Oceanography, 60(3), 353-365, DOI: https://doi.org/10.1590/S1679-87592012000300008
» https://doi.org/10.1590/S1679-87592012000300008
COLLIER, J. L. & PALENIK, B. 2003. Phycoerythrin-containing picoplankton in the Southern California Bight. Deep-Sea Research Part II: Topical Studies in Oceanography, 50(14-16), 2405-2422, DOI: https://doi.org/10.1016/S0967-0645(03)00127-9
» https://doi.org/10.1016/S0967-0645(03)00127-9
COLOMBET, J., FUSTER, M., BILLARD, H. & SIMENGANDO, T. 2020. Femtoplankton: what’s new? Viruses, 12(8), 881.
EDVARSEN, A., ZHOU, M., TANDE, K. S. & ZHU, Y. 2002. Zooplankton population dynamics: measuring in situ growth and mortality rates using an Optical Plankton Counter. Marine Ecolosy Progress Series, 227, 205-219, DOI: http://jstor.org/stable/24864953
» http://jstor.org/stable/24864953
FERNANDES, L. D. A., FAGUNDES NETTO, E. B. & COUTINHO, R. 2017. Inter-annual cascade effect on marine food web: a benthic pathway lagging nutrient supply to pelagic fish stock. PLoS One, 12(9), e0184512, DOI: https://doi.org/10.1371/journal.pone.0184512
» https://doi.org/10.1371/journal.pone.0184512
FERNANDES, L. D. A., QUINTANILHA, J., MONTEIRORIBAS, W., GONZALEZ-RODRIGUEZ, E. & COUTINHO, R. 2012. Seasonal and interannual coupling between sea surface temperature, phytoplankton and meroplankton in the subtropical south-western Atlantic Ocean. Journal of Plankton Research, 34(3), 236-244, DOI: https://doi.org/10.1093/plankt/fbr106
» https://doi.org/10.1093/plankt/fbr106
FLAVIANI, F., SCHROEDER, D. C., LEBRET, K., BALESTRERI, C., HIGHFIELD, A. C., SCHROEDER, J. L., THORPE, S. E., MOORE, K., PASCKIEWICZ, K., PFAFF, M. C., RYBICKI, E. P. & COLEMAN, M. 2018. Distinct oceanic micro-biomes from viruses to protists located near the Antarctic circumpolar current. Frontiers in Microbiology, 9, 1474, DOI: https://doi.org/10.3389/fmicb.2018.01474
» https://doi.org/10.3389/fmicb.2018.01474
FREIRE, K. M. F., ALMEIDA, Z. S., AMADOR, J. R. E. T., ARAGÃO, J. A., ARAÚJO, A. R. R., ÁVILA-DA-SILVA, A. O., BENTES, B., CARNEIRO, M. H., CHIQUIERI, J., FERNANDES, C. A. F., FIGUEIREDO, M. B., HOSTIM-SILVA, M., JIMENEZ, É. A., KEUNECKE, K. A., LOPES, P. F. M., MENDONÇA, J. T., MUSIELLO-FERNANDES, J., OLAVO, G., PRIMITIVO, C., ROTUNDO, M. M., SANTANA, R. F., SANT’ANA, R., SCHEIDT, G., SILVA, L. M. A., TRINDADE-SANTOS, I., VELASCO, G. & VIANNA, M. 2021. Reconstruction of marine commercial landings for the Brazilian industrial and artisanal fisheries from 1950 to 2015. Frontiers in Marine Science, 8, 659110, DOI: https://doi.org/10.3389/fmars.2021.659110
» https://doi.org/10.3389/fmars.2021.659110
FUHRMAN, J. A. 2009. Microbial community structure and its functional implications. Nature, 459(7244), 193-199, DOI: https://doi.org/10.1038/nature08058
» https://doi.org/10.1038/nature08058
GAO, K., BEARDALL, J., HÄDER, D. P., HALL-SPENCER, J. M., GAO, G. & HUTCHINS, D. A. 2019. Effects of ocean acidification on marine photosynthetic organisms under the concurrent influences of warming, UV radiation, and deoxygenation. Frontiers in Marine Science, 6, 322, DOI: https://doi.org/10.3389/fmars.2019.00322
» https://doi.org/10.3389/fmars.2019.00322
GASOL, J. M. 1999. How to count picoalgae and bacteria with the FACScalibur fow cytometer. Counting Picoplankton with FC, 2, 1-33.
GASOL, J. M. & MORÁN, X. A. G. 2015. Flow cytometric determination of microbial abundances and its use to obtain indices of community structure and relative activity. In: MCGENITY, T. J., TIMMIS, K. N. & NOGALES, B. (eds.). Hydrocarbon and lipid microbiology protocols. Single-cell and single-molecule methods Heidelberg: Springer-Verlag, pp. 159-187, DOI: https://doi.org/10.1007/8623_2015_139
» https://doi.org/10.1007/8623_2015_139
GOLDMAN, J. C. 1999. Inorganic carbon availability and the growth of large marine diatoms. Marine Ecology Progress Series, 180, 81-91, DOI: https://doi.org/10.3354/meps180081
» https://doi.org/10.3354/meps180081
GUENTHER, M., GONZALEZ-RODRIGUEZ, E., CARVALHO, W. F., REZENDE, C. E., MUGRABE, G. & VALENTIN, J. L. 2008. Plankton trophic structure and particulate organic carbon production during a coastal downwelling-upwelling cycle. Marine Ecology Progress Series, 363, 109-119, DOI: https://doi.org/10.3354/meps07458
» https://doi.org/10.3354/meps07458
GUENTHER, M. & VALENTIN, J. L. 2008. Bacterial and phytoplankton production in two coastal systems influenced by distinct eutrophication processes. Oecologia Brasiliensis, 12(1), 172-178.
HINGA, K. R. 2002. Effects of pH on coastal marine phytoplankton. Marine Ecology Progress Series, 238, 281-300, DOI: https://doi.org/10.3354/meps238281
» https://doi.org/10.3354/meps238281
HYUN, B., KIM, J. M., JANG, P. G., JANG, M. C., CHOI, K. H., LEE, K., YANG, E. J., NOH, J. H. & SHIN, K. 2020. The effects of ocean acidification and warming on growth of a natural community of coastal phytoplankton. Journal of Marine Science and Engineering, 8(10), 821, DOI: https://doi.org/10.3390/jmse8100821
» https://doi.org/10.3390/jmse8100821
IPCC (Intergovernmental Panel on Climate Change). 2021. Climate Change 2021: the physical science basis Cambridge: Cambridge University Press, DOI: https://doi.org/10.1017/9781009157896
» https://doi.org/10.1017/9781009157896
ISHIDA, H., ISONO, R. S., KITA, J. & WATANABE, Y. W. 2021. Long-term ocean acidification trends in coastal waters around Japan. Scientific Reports, 11(1), 15052, DOI: https://doi.org/10.1038/s41598-021-84657-0
» https://doi.org/10.1038/s41598-021-84657-0
JEFFREY S. W., MANTOURA, R. F. C. & WRIGHT, S. W. 1997. Phytoplankton pigments in oceanography: guidelines to modern methods (Monographs) Paris: Unesco Publishing.
JOVER, L. F., EFFLER, T. C., BUCHAN, A., WILHELM, S. W. & WEITZ, J. S. 2014. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nature Reviews Microbiology, 12(7), 519-528, DOI: https://doi.org/10.1038/nrmicro3289
» https://doi.org/10.1038/nrmicro3289
KARLUSICH, J. J. P., BOWLER, C. & BISWAS, H. 2021. Carbon dioxide concentration mechanisms in natural populations of marine diatoms: insights from Tara oceans. Frontiers in Plant Science, 12, 657821, DOI: https://doi.org/10.3389/fpls.2021.657821
» https://doi.org/10.3389/fpls.2021.657821
KUVALDINA, N., LIPS, I., LIPS, U. & LIBLIK, T. 2010. The influence of a coastal upwelling event on chlorophyll a and nutrient dynamics in the surface layer of the Gulf of Finland, Baltic Sea. Hydrobiologia, 639(1), 221-230, DOI: https://doi.org/10.1007/s10750-009-0022-4
» https://doi.org/10.1007/s10750-009-0022-4
LI, W. K. W. 1994. Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: measurements from fow cytometric sorting. Limnology and Oceanography, 39(1), 169-175.
LIPS, I. & LIPS, U. 2010. Phytoplankton dynamics affected by the coastal upwelling events in the Gulf of Finland in July-August 2006. Journal of Plankton Research, 32(9), 1269-1282, DOI: https://doi.org/10.1093/plankt/fbq049
» https://doi.org/10.1093/plankt/fbq049
LITCHMAN, E., PINTO, P., EDWARDS, K. F., KLAUSMEIER, C. A., KREMER, C. T. & THOMAS, M. K. 2015. Global biogeochemical impacts of phytoplankton: a trait-based perspective. Journal of Ecology, 103(6), 1384-1396, DOI: https://doi.org/10.1111/1365-2745.12438
» https://doi.org/10.1111/1365-2745.12438
LIU, X., FENG, J. & WANG, Y. 2019. Chlorophyll a predictability and relative importance of factors governing lake phytoplankton at diferent timescales. Science of the Total Environment, 648, 472-480, DOI: https://doi.org/10.1016/j.scitotenv.2018.08.146
» https://doi.org/10.1016/j.scitotenv.2018.08.146
MADHU, N. V., ANIL, P., MEENU, P., GIREESHKUMAR, T. R., MURALEEDHARAN, K. R., REHITHA, T. V., DAYANA, M. & VISHAL, C. R. 2021. Response of coastal phytoplankton to upwelling induced hydrological changes in the Alappuzha mud bank region, southwest coast of India. Oceanologia, 63(2), 261-275, DOI: https://doi.org/10.1016/j.oceano.2021.02.001
» https://doi.org/10.1016/j.oceano.2021.02.001
MAHIQUES, M. M., BÍCEGO, M. C., SILVEIRA, I. C. A., SOUSA, S. H. M., LOURENÇO, R. A. & FUKUMOTO, M. M. 2005. Modem sedimentation in the Cabo Frio up-welling system, Southeastern Brazilian shelf. Anais da Academia Brasileira de Ciências, 77(3), 535-548, DOI: https://doi.org/10.1590/s0001-37652005000300013
» https://doi.org/10.1590/s0001-37652005000300013
MALITS, A., BORAS, J. A., BALAGUÉ, V., CALVO, E., GASOL, J. M., MARRASÉ, C., PELEJERO, C., PINHASSI, J., SALA, M. M. & VAQUÉ, D. 2021. Viral-mediated microbe mortality modulated by ocean acidification and eutrophication: consequences for the carbon fluxes through the microbial food web. Frontiers in Microbiology, 12, 635821, DOI: https://doi.org/10.3389/fmicb.2021.635821
» https://doi.org/10.3389/fmicb.2021.635821
MARIE, D., BRUSSAARD, C. P. D., THYRHAUG, R., BRATBAK, G. & VAULOT, D. 1999. Enumeration of marine viruses in culture and natural samples by fow cytometry. Applied and Environmental Microbiology, 65(1), 45-52, DOI: https://doi.org/10.1128/aem.65.1.45-52.1999
» https://doi.org/10.1128/aem.65.1.45-52.1999
MOREIRA, D. & LÓPEZ-GARCÍA, P. 2019. Time series are critical to understand microbial plankton diversity and ecology. Molecular Ecology, 28(5), 920-922, DOI: https://doi.org/10.1111/mec.15015
» https://doi.org/10.1111/mec.15015
OLIVEIRA, R. R., PEZZI, L. P., SOUZA, R. B., SANTINI, M. F., CUNHA, L. C. & PACHECO, F. S. 2019. First measurements of the ocean-atmosphere CO2 fluxes at the Cabo Frio upwelling system region, Southwestern Atlantic Ocean. Continental Shelf Research, 181, 135-142, DOI: https://doi.org/10.1016/j.csr.2019.05.008
» https://doi.org/10.1016/j.csr.2019.05.008
PLATT, T. & DENMAN K. 1977. Organisation in the pelagic ecosystem. Helgolander Wiss Meeresunters, 30, 575-558.
PEDROTTI, M. L., MOUSSEAU, L., MARRO, S., PASSAFIUME, O., GOSSAERT, M. & LABAT, J. P. 2017. Variability of ultraplankton composition and distribution in an oligotrophic coastal ecosystem of the NW Mediterranean Sea derived from a two-year survey at the single cell level. PLoS One, 12(12), e0190121, DOI: https://doi.org/10.1371/journal.pone.0190121
» https://doi.org/10.1371/journal.pone.0190121
PEREIRA, G. C., GRANATO, A., FIGUEIREDO, A. R. & EBECKEN, N. F. F. 2009. Virioplankton abundance in trophic gradients of an upwelling feld. Brazilian Journal of Microbiology, 40(4), 857-865, DOI: https://doi.org/10.1590/S1517-83822009000400017
» https://doi.org/10.1590/S1517-83822009000400017
PRUDER, G. D. & BOLTON, E. T. 1979. The role of CO2 enrichment of aerating gas in the growth of an estuarine diatom. Aquaculture, 17(1), 1-15, DOI: https://doi.org/10.1016/0044-8486(79)90133-9
» https://doi.org/10.1016/0044-8486(79)90133-9
PUSCEDDU, A., DELL’ANNO, A., FABIANO, M. & DANOVARO, R. 2009. Quantity and bioavailability of sediment organic matter as signatures of benthic trophic status. Marine Ecology Progress Series, 375, 41-52, DOI: https://doi.org/10.3354/meps07735
» https://doi.org/10.3354/meps07735
RAI, S. V. & RAJASHEKHAR, M. 2014. Effect of pH, salinity and temperature on the growth of six species of marine phytoplankton. Journal of Algal Biomass Utilization, 5(4), 55-59.
RIBEIRO, C. G., SANTOS, A. L., MARIE, D., PELLIZARI, V. H., BRANDINI, F. P. & VAULOT, D. 2016. Pico and nanoplankton abundance and carbon stocks along the Brazilian Bight. PeerJ, 2016(11), e2587, DOI: https://doi.org/10.7717/peerj.2587
» https://doi.org/10.7717/peerj.2587
ROUBEYRIE, L. & CELLES, S. 2018. Windrose: a python matplotlib, numpy library to manage wind and pollution data, draw windrose. Journal of Open Source Software, 3(29), 268, DOI: https://doi.org/10.21105/joss.00268
» https://doi.org/10.21105/joss.00268
SATHISH, K., PATIL, J. S. & ANIL, A. C. 2020. Phytoplankton chlorophyll-breakdown pathway: Implication in ecosystem assessment. Journal of Environmental Management, 258, 109989, DOI: https://doi.org/10.1016/j.jenvman.2019.109989
» https://doi.org/10.1016/j.jenvman.2019.109989
SHI, D., XU, Y., HOPKINSON, B. M. & MOREL, F. M. M. 2010. Effect of ocean acidification on iron availability to marine phytoplankton. Science, 327(5966), 676-679, DOI: https://doi.org/10.1126/science.1183517
» https://doi.org/10.1126/science.1183517
STRICKLAND, J. D. & PARSONS, T. R. 1972. A practical handbook of seawater analysis. Fisheries Research Board of Canada Bulletin, 167(7), 405, DOI: https://doi.org/10.2307/1979241
» https://doi.org/10.2307/1979241
WEINBAUER, M. G. & RASSOULZADEGAN, F. 2004. Are viruses driving microbial diversification and diversity? Environmental Microbiology, 6(1), 1-11, DOI: https://doi.org/10.1046/j.1462-2920.2003.00539.x
» https://doi.org/10.1046/j.1462-2920.2003.00539.x
WIEKING, G. & KRÖNCKE, I. 2005. Is benthic trophic structure affected by food quality? The Dogger Bank example. Marine Biology, 146(2), 387-400, DOI: https://doi.org/10.1007/s00227-004-1443-2
» https://doi.org/10.1007/s00227-004-1443-2
WILHELM, S. W. & SUTTLE, C. A. 1999. Nutrient cycles the. Bioscience, 49(10), 781-788.
WOMMACK, K. E. & COLWELL, R. R. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews, 64(1), 69-114, DOI: https://doi.org/10.1128/mmbr.64.1.69-114.2000
» https://doi.org/10.1128/mmbr.64.1.69-114.2000
WOOD, S. N. 2017. Generalized additive models: an introduction with R 2nd ed. New York: Chapman and Hall/CRC, DOI: https://doi.org/10.1201/9781315370279
» https://doi.org/10.1201/9781315370279
XIE, L., WEI, W., CAI, L., CHEN, X., HUANG, Y., JIAO, N., ZHANG, R. & LUO, Y. W. 2020. A global viral oceanography database (gVOD). Earth System Science Data Discussions, 13, 1-22, DOI: https://doi.org/10.5194/essd-2020-120
» https://doi.org/10.5194/essd-2020-120
XU, Y., SHI, D., ARISTILDE, L. & MOREL, F. M. M. 2012. The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: Possible role of weak complexes. Limnology and Oceanography, 57(1), 293-304, DOI: https://doi.org/10.4319/lo.2012.57.1.0293
» https://doi.org/10.4319/lo.2012.57.1.0293
YANG, Y., GU, X., TE, S. H., GOH, S. G., MANI, K., HE, Y. & GIN, K. Y. H. 2019. Occurrence and distribution of viruses and picoplankton in tropical freshwater bodies determined by flow cytometry. Water Research, 149, 342-350, DOI: https://doi.org/10.1016/j.watres.2018.11.022
» https://doi.org/10.1016/j.watres.2018.11.022
ZAR, J. H. 2010. Biostatistical analysis New Jersey: Pearson Prentice Hall.
ZUUR, A. F., IENO, E. N. & ELPHICK, C. S. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution, 1(1), 3-14, DOI: https://doi.org/10.1111/j.2041-210x.2009.00001.x