More stories

  • in

    Antixenosis in Glycine max (L.) Merr against Acyrthosiphon pisum (Harris)

    1.Pagano, M. C. & Miransari, M. The importance of soybean production worldwide. In Abiotic and Biotic Stresses in Soybean Production Vol. 1 (ed. Miransari, M.) 1–26 (Academic Press, 2016).
    Google Scholar 
    2.FAOSTAT. Food and Agriculture Organisation Statistical Database http://www.apps.fao.org/faostat. Accessed 23 May 2021.3.MacDonald, R. S. et al. Environmental influences on isoflavones and saponins in soybeans and their role in colon cancer. J. Nutr. 135, 1239–1242 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    4.Tidke, S. A. et al. Assessment of anticancer, anti-inflammatory and antioxidant properties of isoflavones present in soybean. Res. J. Phytochem. 12, 35–42 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    5.Hill, J. H. & Whitham, S. A. Control of virus diseases in soybeans. Adv. Virus Res. 90, 355–390 (2014).PubMed 
    Article 

    Google Scholar 
    6.Tian, B. et al. Host adaptation of soybean dwarf virus following serial passages on pea (Pisum sativum) and soybean (Glycine max). Viruses 9, 155 (2017).PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 
    7.Wang, R. Y., Kritzman, A., Hershman, D. E. & Ghabrial, S. A. Aphis glycines as a vector of persistently and nonpersistently transmitted viruses and potential risks for soybean and other crops. Plant Dis. 90, 920–926 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Hesler, L. S., Dashiell, E., Jonathan, A. E. & Lundgren, G. Characterization of resistance to Aphis glycines in soybean accessions. Euphytica 154, 91–99 (2007).Article 

    Google Scholar 
    9.Baldin, E. L. L. et al. Feeding behavior of Aphis glycines (Hemiptera: Aphididae) on soybeans exhibiting antibiosis, antixenosis, and tolerance resistance. Fla. Entomol. 101, 223–228 (2018).Article 

    Google Scholar 
    10.Chang, H.-X. & Hartman, G. L. Characterization of insect resistance loci in the USDA soybean germplasm collection using genome-wide association studies. Front. Plant Sci. 8, 670. https://doi.org/10.3389/fpls.2017.00670 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Bansal, R., Mian, M. A. R. & Michel, A. Characterizing resistance to soybean aphid (Hemiptera: Aphididae): Antibiosis and antixenosis assessment. J. Econ. Entomol. https://doi.org/10.1093/jee/toab038 (2021).Article 
    PubMed 

    Google Scholar 
    12.Klein, A. T. et al. Investigation of the chemical interface in the soybean−aphid and rice−bacteria interactions using MALDI-Mass Spectrometry Imaging. Anal. Chem. 87, 5294–5301 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Hohenstein, J. D. et al. Transcriptional and chemical changes in soybean leaves in response to long-term aphid colonization. Front. Plant Sci. 10, 310 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Blackman, R. L. & Eastop, V. F. Taxonomic issues. In Aphids as Crop Pests (eds van Emden, H. F. & Harrington, R.) 1–36 (CABI, 2017).
    Google Scholar 
    15.Wale, M., Jembere, B. & Seyoum, E. Occurrence of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) on wild leguminous plants in West Gojam, Ethiopia, Sinet. Ethiopian J. Sci. 26, 83–87 (2003).
    Google Scholar 
    16.Chan, C. K., Forbes, A. R. & Raworth, D. A. Aphid-transmitted viruses and their vectors of the world. Agric. Can. Tech. Bull. 3E, 1–216 (1991).
    Google Scholar 
    17.Rashed, A. et al. Vector-borne viruses of pulse crops, with a particular emphasis on North American cropping system. Ann. Entomol. Soc. Am. 111, 205–227 (2018).CAS 
    Article 

    Google Scholar 
    18.Stavrinides, J., McCloskey, J. K. & Ochman, H. Pea Aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl. Environ. Microbiol. 75, 2230–2235 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Peccoud, J., Ollivier, A., Plantegenest, M. & Simon, J.-C. A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. PNAS 106, 7495–7500 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Caillaud, M. C. & Via, S. Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am. Nat. 156, 606–621 (2000).PubMed 
    Article 

    Google Scholar 
    21.Ferrari, J., Godfray, H. C., Faulconbridge, A. S., Prior, K. & Via, S. Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution 60, 1574–1584 (2006).PubMed 
    Article 

    Google Scholar 
    22.Mitku, G. & Damte, T. Development, reproduction, and host preference of Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) on selected lentil genotypes and resistance index of these selected lentil genotypes to pea aphid. Int. J. Entomol. Res. 4, 16–22 (2019).
    Google Scholar 
    23.Powell, G., Tosh, C. R. & Hardie, J. Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 51, 309–330 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Kordan, B. et al. European yellow lupine Lupinus luteus and narrow-leaf lupine Lupinus angustifolius as hosts for the pea aphid Acyrthosiphon pisum. Entomol. Exp. Appl. 128, 139–146 (2008).Article 

    Google Scholar 
    25.Kordan, B. et al. Susceptibility of forage legumes to infestation by the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae). Crop Pasture Sci. 69, 775–784 (2018).Article 

    Google Scholar 
    26.Kordan, B. et al. Antixenosis potential in pulses against the pea aphid (Hemiptera: Aphididae). J. Econ. Entomol. 112, 465–474 (2019).PubMed 
    Article 

    Google Scholar 
    27.Pettersson, J., Tjallingii, W. F. & Hardie, J. Host-plant selection and feeding. In Aphids as Crop Pests (eds van Emden, H. F. & Harrington, R.) 173–195 (CABI, 2017).Chapter 

    Google Scholar 
    28.Martin, B., Collar, J. L., Tjallingi, W. F. & Fereres, A. Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J. Gen. Virol. 78, 2701–2705 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Garzo, E., Moreno, A., Plaza, M. & Fereres, A. Feeding behavior and virus-transmission ability of insect vectors exposed to systemic insecticides. Plants 9, 895. https://doi.org/10.3390/plants9070895 (2020).CAS 
    Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    30.Onstad, D. W. & Knolhoff, L. Arthropod resistance to crops. In Insect Resistance Management (ed. Onstad, D. W.) 293–326 (Academic Press, 2014).Chapter 

    Google Scholar 
    31.Smith, C. M. & Clement, S. L. Molecular bases of plant resistance to arthropods. Annu. Rev. Entomol. 57, 309–328 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Stout, M. J. Reevaluating the conceptual framework for applied research on host-plant resistance. Insect Sci. 20, 263–272 (2013).PubMed 
    Article 

    Google Scholar 
    33.Smith, C. M. & Chuang, W. P. Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Manag. Sci. 70, 528–540 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    34.Dogimont, C., Bendahmane, A., Chovelon, V. & Boissot, N. Host plant resistance to aphids in cultivated crops: Genetic and molecular bases, and interactions with aphid populations. C. R. Biol 333, 566–573 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Chandran, P. et al. Feeding behavior comparison of soybean aphid (Hemiptera: Aphididae) biotypes on different soybean genotypes. J. Econ. Entomol. 106, 2234–2240 (2013).PubMed 
    Article 

    Google Scholar 
    36.Simmonds, M. S. J. Flavonoid-insect interactions: Recent advances in our knowledge. Phytochemistry 64, 21–30 (2003).CAS 
    Article 

    Google Scholar 
    37.Mai, V. C. et al. Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci. 221–222, 1–12 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    38.Morkunas, I. et al. Pea aphid infestation induces changes in flavonoids, antioxidative defence, soluble sugars and sugar transporter expression in leaves of pea seedlings. Protoplasma 253, 1063–1079 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Woźniak, A. et al. The dynamics of the defense strategy of pea induced by exogenous nitric oxide in response to aphid infestation. Int. J. Mol. Sci. 18, 329. https://doi.org/10.3390/ijms18020329 (2017).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    40.Buer, C. S., Muday, G. K. & Djordjevic, M. A. Implications of long-distance flavonoid movement in Arabidopsis thaliana. Plant Signal. Behav. 3, 415–417 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Petrussa, E. et al. Plant flavonoids: Biosynthesis, transport and involvement in stress responses. Int. J. Mol. Sci. 14, 14950–14973 (2013).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    42.Zhao, J. Flavonoid transport mechanisms: How to go, and with whom. Trends Plant Sci. 20, 576–585 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Alseekh, S., de Souza, L. P., Benina, M. & Fernie, A. L. The style and substance of plant flavonoid decoration; Towards defining both structure and function. Phytochemistry 174, 112347. https://doi.org/10.1016/j.phytochem.2020.112347 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Klingauf, F. A. Host plant finding and acceptance. In Aphids, Their Biology, Natural Enemies and Control Vol. 2 (eds Minks, A. K. & Harrewijn, P.) 209–223 (Elsevier, 1987).
    Google Scholar 
    45.Tjallingii, W. F. & Mayoral, A. M. Criteria for host plant acceptance by aphids. In Proceeding 8th International Symposium Insect–Plant Relationships (eds Menken, S. B. J. et al.) 280–282 (Kluwer Academic Publishers, 1992).Chapter 

    Google Scholar 
    46.Wensler, R. J. & Filshie, B. K. Gustatory sense organs in the food canal of aphids. J. Morph. 129, 473–492 (1969).Article 

    Google Scholar 
    47.Gabryś, B. & Tjallingii, W. F. The role of sinigrin in host plant recognition by aphids during initial plant penetration. Entomol. Exp. Appl. 104, 89–93 (2002).Article 

    Google Scholar 
    48.Philippi, J. et al. Correlation of the alkaloid content and composition of narrow-leafed lupins (Lupinus angustifolius L.) to aphid susceptibility. J. Pest Sci. 89, 359–373 (2016).Article 

    Google Scholar 
    49.Van Hoof, H. A. An investigation of the biological transmission of a non-persistent virus. Doctoral thesis (Van Putten and Oortmijer, 1958).50.Dancewicz, K., Szumny, A., Wawrzeńczyk, C. & Gabryś, B. Repellent and antifeedant activities of citral-derived lactones against the peach potato aphid. Int. J. Mol. Sci. 21, 8029. https://doi.org/10.3390/ijms21218029 (2020).CAS 
    Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    51.Kordan, B. et al. Variation in susceptibility of rapeseed cultivars to the peach potato aphid. J. Pest. Sci. 94, 435–449 (2021).Article 

    Google Scholar 
    52.Pritchard, J. & Vickers, L. H. Aphids and stress. In Aphids as Crop Pests (eds Van Emden, H. F. & Harrington, R.) 132–147 (CABI, 2017).Chapter 

    Google Scholar 
    53.Pompon, J. & Pelletier, Y. Changes in aphid probing behaviour as a function of insect age and plant resistance level. Bull. Entomol. Res. 102, 550–557 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    54.van Emden, H. F. Host-plant resistance. In Aphids as Crop Pests (eds van Emden, H. F. & Harrington, R.) 515–532 (CABI, 2017).Chapter 

    Google Scholar 
    55.Gould, K. S. & Lister, C. Flavonoid functions in plants. In Flavonoids, Chemistry, Biochemistry and Applications (eds Andersen, Ø. M. & Markham, K. R.) 397–442 (CRC Press, 2006).
    Google Scholar 
    56.Goławska, S., Kapusta, I., Łukasik, I. & Wójcicka, A. Effect of phenolics on the pea aphid, Acyrthosiphon pisum (Harris) population on Pisum sativum L. (Fabaceae). Pestycydy. 3–4, 71–77 (2008).
    Google Scholar 
    57.Goławska, S. & Łukasik, I. Antifeedant activity of luteolin and genistein against the pea aphid, Acyrthosiphon pisum. J. Pest Sci. 85, 443–450 (2012).Article 

    Google Scholar 
    58.Goławska, S. et al. Alfalfa (Medicago sativa L.) apigenin glycosides and their effect on the pea aphid (Acyrthosiphon pisum). Polish J. Environ. Stud. 19, 913–919 (2010).
    Google Scholar 
    59.Johnson, A. D. & Singh, A. Larvicidal activity and biochemical effects of apigenin against filarial vector Culex quinquefasciatus. Int. J. Life. Sci. Sci. Res. 3, 1315–1321 (2017).
    Google Scholar 
    60.Boué, S. M. & Raina, A. K. Effects of plant flavonoids on fecundity, survival, and feeding of the formosan subterranean termite. J. Chem. Ecol. 29, 2575–2584 (2003).PubMed 
    Article 

    Google Scholar 
    61.Xu, D. et al. Antifeedant activities of secondary metabolites from Ajuga nipponensis against adult of striped flea beetles, Phyllotreta striolata. J. Pest Sci. 82, 195–202 (2009).Article 

    Google Scholar 
    62.Goławska, S., Sprawka, I. & Łukasik, I. Effect of saponins and apigenin mixtures on feeding behavior of the pea aphid, Acyrthosiphon pisum Harris. Biochem. Syst. Ecol. 55, 137–144 (2014).Article 
    CAS 

    Google Scholar 
    63.Zavala, J. A., Scopel, A. L. & Ballaré, C. L. Effects of ambient UV-B radiation on soybean crops: Impact on leaf herbivory by Anticarsia gemmatalis. Plant Ecol. 156, 121–130 (2001).Article 

    Google Scholar 
    64.Bentivenha, J. P. F. et al. Role of the rutin and genistein flavonoids in soybean resistance to Piezodorus guildinii (Hemiptera: Pentatomidae). Arthropod Plant Interact. 12, 311–320 (2018).Article 

    Google Scholar 
    65.Hoffmann-Campo, C. B., Harborne, J. B. & McCaffery, A. R. Pre-ingestive and post-ingestive effects of soya bean extracts and rutin on Trichoplusia ni growth. Entomol. Exp. Appl. 98, 181–194 (2001).Article 

    Google Scholar 
    66.Yuan, E. et al. Increases in genistein in Medicago sativa confer resistance against the Pisum host race of Acyrthosiphon pisum. Insects. 10, 97. https://doi.org/10.3390/insects10040097 (2019).Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    67.Meng, F. et al. QTL underlying the resistance to soybean aphid (Aphis glycines Matsumura) through isoflavone-mediated antibiosis in soybean cultivar ‘Zhongdou 27’. Theor Appl. Genet. 123, 1459–1465 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Murakami, S. et al. Insect-induced daidzein, formononetin and their conjugates in soybean leaves. Metabolites 4, 532–546 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    69.Lattanzio, V. et al. Role of endogenous flavonoids in resistance mechanism of Vigna to aphids. J. Agric. Food Chem. 48, 5316–5320 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Delgado-Núñez, E. J. et al. Isorhamnetin: A nematocidal flavonoid from Prosopis laevigata leaves against Haemonchus contortus eggs and larvae. Biomolecules 10, 773 (2020).PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 
    71.Gómez, J. D., Vital, C. E., Oliveira, M. G. A. & Ramos, H. J. O. Broad range flavonoid profiling by LC/MS of soybean genotypes contrasting for resistance to Anticarsia gemmatalis (Lepidoptera: Noctuidae). PLoS ONE https://doi.org/10.1371/journal.pone.0205010 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Khan, M. A. M., Ulrichs, C. & Mewis, I. Effect of water stress and aphid herbivory on flavonoids in broccoli (Brassica oleracea var. italica Plenck). J. Appl. Bot. Food Qual. 84, 178–182 (2011).CAS 

    Google Scholar 
    73.Bale, J. S., Ponder, K. L. & Pritchard, J. Coping with stress. In Aphids as Crop Pests (eds van Emden, H. F. & Harrington, R.) 287–309 (CABI, 2007).Chapter 

    Google Scholar 
    74.Atteyat, M., Abu-Romman, S., Abu-Darwish, M. & Ghabeish, I. Impact of flavonoids against woolly apple aphid, Eriosoma lanigerum (Hausmann) and its sole parasitoid, Aphelinus mali (Hald). J. Agric. Sci. 4, 227–236 (2012).
    Google Scholar 
    75.Tjallingii, W. F. & Hogen Esch, T. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18, 317–328 (1993).Article 

    Google Scholar 
    76.Cherqui, A. & Tjallingii, W. F. Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J. Insect Physiol. 46, 1177–1186 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Silva-Sanzana, C., Estevez, J. M. & Blanco-Herrera, F. Influence of cell wall polymers and their modifying enzymes during plant–aphid interactions. J. Exp. Bot. 71, 3854–3864 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    78.Alvarez, A. E. et al. Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to aphid Myzus persicae. Entomol. Exp. Appl. 121, 145–157 (2006).Article 

    Google Scholar 
    79.Alvarez, A. E. et al. Infection of potato plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae. Entomol. Exp. Appl. 125, 135–144 (2007).Article 

    Google Scholar 
    80.Machado-Assefh, C. R. & Alvarez, A. E. Probing behavior of aposymbiotic green peach aphid (Myzus persicae) on susceptible Solanum tuberosum and resistant Solanum stoloniferum plants. Insect Sci. 25, 127–136 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    81.Common Catalogue of Varieties of Agricultural Plant Species [CCA]. 37th complete edition. Official Journal of the European Union C 13/1 (2019). Accessed 23 May 2021.82.Porejestrowe doświadczalnictwo odmianowe. Charakterystyka odmian. http://www.coboru.gov.pl/Polska/Rejestr/odm_w_rej.aspx?kodgatunku=SOS. Accessed 23 May 2021.83.Meier, U. Growth stages of mono- and dicotyledonous plants: BBCH. Monograph (Julius Kühn-Institut, 2018).84.Beer, K., Joschinski, J., Sastre, A. A., Kraus, J. & Helfrich-Forster, C. A damping circadian clock drives weak oscillations in metabolism and locomotor activity of aphids (Acyrthosiphon pisum). Sci. Rep. 7, 1–5. https://doi.org/10.1038/s41598-017-15014-3 (2017).CAS 
    Article 

    Google Scholar 
    85.Joschinski, J., Beer, K., Helfrich-Forster, C. & Krauss, J. Pea aphids (Hemiptera: Aphididae) have diurnal rhythms when raised independently of a host plant. J. Insect. Sci. 16, 1–5 (2016).Article 

    Google Scholar 
    86.Graham, T. L. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol. 95, 594–603 (1991).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    87.Lee, J. H. et al. Characterization of isoflavones accumulation in developing leaves of soybean (Glycine max) cultivars. J. Korean Soc. Appl. Biol. Chem. 52(2), 139–143 (2009).CAS 
    Article 

    Google Scholar 
    88.Magarelli, G. et al. Rutin and total isoflavone determination in soybean at different growth stages by using voltammetric methods. Microchem. J. 117, 149–155 (2014).CAS 
    Article 

    Google Scholar 
    89.Perlatti, B. et al. Application of a quantitative HPLC-ESI-MS/MS method for flavonoids in different vegetables matrices. J. Braz. Chem. Soc. 27(3), 475–483 (2016).CAS 

    Google Scholar 
    90.Biesaga, M. & Pyrzyńska, K. Stability of bioactive polyphenols from honey during different extraction methods. Food Chem. 136, 46–54 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    91.Sergiel, I., Pohl, P. & Biesaga, M. Characterisation of honeys according to their content of phenolic compounds using high performance liquid chromatography/tandem mass spectrometry. Food Chem. 145, 404–408 (2014).CAS 
    PubMed 
    Article 

    Google Scholar  More

  • in

    The bifidobacterial distribution in the microbiome of captive primates reflects parvorder and feed specialization of the host

    1.Arbour, J. H. & Santana, S. E. A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity. Evolution 71, 1600–1613 (2017).PubMed 
    Article 

    Google Scholar 
    2.Groves, C. Primates (Taxonomy) in The International Encyclopedia of Primatology (ed Augustin Fuentes) (John Wiley & Sons, Inc., 2016).3.Cotton, A., Clark, F., Boubli, J. & Schwitzer, C. IUCN red list of threatened primate species in An Introduction to Primate Conservation 31–18 (Oxford University Press, 2016).
    Google Scholar 
    4.Stumpf, R. M. et al. Microbiomes, metagenomics, and primate conservation: New strategies, tools, and applications. Biol. Conserv. 199, 56–66 (2016).Article 

    Google Scholar 
    5.West, A. G. et al. The microbiome in threatened species conservation. Biol. Conserv. 229, 85–98 (2019).Article 

    Google Scholar 
    6.Cunningham, A. A., Daszak, P. & Wood, J. L. N. One Health, emerging infectious diseases and wildlife: two decades of progress?. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160167 (2017).Article 

    Google Scholar 
    7.Ramey, A. M. & Ahlstrom, C. A. Antibiotic resistant bacteria in wildlife: Perspectives on trends, acquisition and dissemination, data gaps, and future directions. J. Wildl. Dis. 56, 1–15 (2020).PubMed 
    Article 

    Google Scholar 
    8.Clayton, J. B. et al. Captivity humanizes the primate microbiome. Proc. Natl. Acad. Sci. 113, 10376–10381 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Hale, V. L. et al. Gut microbiota in wild and captive Guizhou snub-nosed monkeys. Rhinopithecus brelichi. Am. J. Primatol. 81, e22989 (2019).CAS 
    PubMed 

    Google Scholar 
    10.Kriss, M., Hazleton, K. Z., Nusbacher, N. M., Martin, C. G. & Lozupone, C. A. Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Curr. Opin. Microbiol. 44, 34–40 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Mahnert, A. et al. Man-made microbial resistances in built environments. Nat. Commun. 10, 1–12 (2019).CAS 
    Article 

    Google Scholar 
    12.Amato, K. R. et al. Using the gut microbiota as a novel tool for examining colobine primate GI health. Glob. Ecol. Conserv. 7, 225–237 (2016).Article 

    Google Scholar 
    13.Zhu, H. et al. Diarrhea-associated intestinal microbiota in captive Sichuan golden snub-nosed monkeys (Rhinopithecus roxellana). Microbes Environ. ME17163 (2018).14.Campbell, T. P. et al. The microbiome and resistome of chimpanzees, gorillas, and humans across host lifestyle and geography. ISME J. 14, 1584–1599 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Buzzard, P. J. Ecological partitioning of Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest. Int. J. Primatol. 27, 529–558 (2006).Article 

    Google Scholar 
    16.Chapman, C. A. et al. The guenons: diversity and adaptation in African monkeys. 325–350 (Springer, 2004).17.Krishnadas, M., Chandrasekhara, K. & Kumar, A. The response of the frugivorous lion-tailed macaque (Macaca silenus) to a period of fruit scarcity. Am. J. Primatol. 73, 1250–1260 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Swedell, L., Hailemeskel, G. & Schreier, A. Composition and seasonality of diet in wild hamadryas baboons: preliminary findings from Filoha. Folia Primatol. 79, 476–490 (2008).Article 

    Google Scholar 
    19.Basabose, A. K. Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. Am. J. Primatol. 58, 1–21 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.McLennan, M. R. & Ganzhorn, J. U. Nutritional characteristics of wild and cultivated foods for chimpanzees (Pan troglodytes) in agricultural landscapes. Int. J. Primatol. 38, 122–150 (2017).Article 

    Google Scholar 
    21.Newton-Fisher, N. E. The diet of chimpanzees in the Budongo Forest Reserve Uganda. Afr. J. Ecol. 37, 344–354 (1999).Article 

    Google Scholar 
    22.Bach, T. H., Chen, J., Hoang, M. D., Beng, K. C. & Nguyen, V. T. Feeding behavior and activity budget of the southern yellow-cheeked crested gibbons (Nomascus gabriellae) in a lowland tropical forest. Am. J. Primatol. 79, e22667 (2017).Article 

    Google Scholar 
    23.Fan, P.-F., Fei, H.-L., Scott, M. B., Zhang, W. & Ma, C.-Y. Habitat and food choice of the critically endangered cao vit gibbon (Nomascus nasutus) in China: implications for conservation. Biol. Conserv. 144, 2247–2254 (2011).Article 

    Google Scholar 
    24.Fan, P. F., Fei, H. L. & Ma, C. Y. Behavioral responses of cao vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi China. Am. J. Primatol. 74, 632–641 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.McConkey, K. R., Ario, A., Aldy, F. & Chivers, D. J. Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu Central Kalimantan. Int. J. Primatol. 24, 19–32 (2003).Article 

    Google Scholar 
    26.Amora, T. D., BeltrÃO-Mendes, R. & Ferrari, S. F. Use of alternative plant resources by common marmosets (Callithrix jacchus) in the semi-arid Caatinga scrub forests of northeastern Brazil. Am. J. Primatol. 75, 333–341 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Dietz, J. M., Peres, C. A. & Pinder, L. Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia). Am. J. Primatol. 41, 289–305 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Garber, P. A. Feeding ecology and behaviour of the genus Saguinus. Marmosets and tamarins: systematics behaviour and ecology (1993).29.Heymann, E. W., Knogge, C. & Tirado Herrera, E. R. Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis. Am. J. Primatol. 51, 153–158 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Porter, L. M. Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int. J. Primatol. 22, 961–992 (2001).Article 

    Google Scholar 
    31.Anapol, F. & Lee, S. Morphological adaptation to diet in platyrrhine primates. Am. J. Phys. Anthropol. 94, 239–261 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Nash, L. T. Dietary, behavioral, and morphological aspects of gummivory in primates. Am. J. Phys. Anthropol. 29, 113–137 (1986).Article 

    Google Scholar 
    33.Abreu, F., De la Fuente, M. F. C., Schiel, N. & Souto, A. Feeding ecology and behavioral adjustments: flexibility of a small neotropical primate (Callithrix jacchus) to survive in a semiarid environment. Mammal Res. 61, 221–229 (2016).Article 

    Google Scholar 
    34.Cunha, A. A., Vieira, M. V. & Grelle, C. E. V. Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic forest fragment: the capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca forest Rio de Janeiro. Urban Ecosyst. 9, 351–359 (2006).Article 

    Google Scholar 
    35.Passamani, M. & Rylands, A. B. Feeding behavior of Geoffroy’s marmoset (Callithrix geoffroyi) in an Atlantic forest fragment of south-eastern Brazil. Primates 41, 27–38 (2000).PubMed 
    Article 

    Google Scholar 
    36.Veracini, C. Habitat use and ranging behavior of the silvery marmoset (Mico argentatus) at Caxiuanã National Forest (eastern Brazilian Amazonia) in The smallest anthropoids 221–240 (Springer, 2009).37.Yépez, P., De La Torre, S. & Snowdon, C. T. Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am. J. Primatol. 66, 145–158 (2005).PubMed 
    Article 

    Google Scholar 
    38.Hale, V. L. et al. Diet versus phylogeny: a comparison of gut microbiota in captive colobine monkey species. Microb. Ecol. 75, 515–527 (2018).PubMed 
    Article 

    Google Scholar 
    39.Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Frankel, J. S., Mallott, E. K., Hopper, L. M., Ross, S. R. & Amato, K. R. The effect of captivity on the primate gut microbiome varies with host dietary niche. Am. J. Primatol. 81, e23061 (2019).PubMed 
    Article 

    Google Scholar 
    41.McKenzie, V. J. et al. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57, 690–704 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Lugli, G. A. et al. Evolutionary development and co‐phylogeny of primate‐associated bifidobacteria. Environ. Microbiol. (2020).43.Milani, C. et al. Unveiling bifidobacterial biogeography across the mammalian branch of the tree of life. ISME J. 11, 2834–2847 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Lugli, G. A. et al. Comparative genomic and phylogenomic analyses of the Bifidobacteriaceae family. BMC Genom. 18, 568 (2017).Article 
    CAS 

    Google Scholar 
    45.Pokusaeva, K., Fitzgerald, G. F. & van Sinderen, D. Carbohydrate metabolism in Bifidobacteria. Genes Nutr. 6, 285–306 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Stewart, C. J. et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 562, 583–588 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Orkin, J. D. et al. Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest. ISME J. 13, 183–196 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Neuzil-Bunesova, V. et al. Five novel bifidobacterial species isolated from faeces of primates in two Czech zoos: Bifidobacterium erythrocebi sp. nov., Bifidobacterium moraviense sp. nov., Bifidobacterium oedipodis sp. nov., Bifidobacterium olomucense sp. nov. and Bifidobacterium panos sp. nov. Int. J. Syst. Evol. Microbiol. (2020).49.Duranti, S. et al. Characterization of the phylogenetic diversity of two novel species belonging to the genus Bifidobacterium: Bifidobacterium cebidarum sp. Nov. and Bifidobacterium leontopitheci sp. nov.. Int. J. Syst. Evol. Microbiol. 70, 2288–2297 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    50.Modesto, M. et al. Bifidobacterium primatium sp. nov., Bifidobacterium scaligerum sp. nov., Bifidobacterium felsineum sp. nov. and Bifidobacterium simiarum sp. nov.: Four novel taxa isolated from the faeces of the cotton top tamarin (Saguinus oedipus) and the emperor tamarin (Saguinus imperator). Syst. Appl. Microbiol. (2018).51.Neuzil-Bunesova, V. et al. Bifidobacterium canis sp nov a novel member of the Bifidobacterium pseudolongum phylogenetic group isolated from faeces of a dog (Canis lupus f. familiaris). Int. J. Syst. Evol. Microbiol. 70, 5040–5047 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Vlková, E. et al. A new medium containing mupirocin, acetic acid, and norfloxacin for the selective cultivation of bifidobacteria. Anaerobe 34, 27–33 (2015).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    53.Carding, S., Verbeke, K., Vipond, D. T., Corfe, B. M. & Owen, L. J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 26, 26191 (2015).
    Google Scholar 
    54.WagnerMackenzie, B. et al. Bacterial community collapse: a meta-analysis of the sinonasal microbiota in chronic rhinosinusitis. Environ. Microbiol. 19, 381–392 (2017).CAS 
    Article 

    Google Scholar 
    55.Arboleya, S., Watkins, C., Stanton, C. & Ross, R. P. Gut bifidobacteria populations in human health and aging. Front. Microbiol. 7 (2016).56.Binda, C. et al. Actinobacteria: a relevant minority for the maintenance of gut homeostasis. Dig. Liver Dis. 50, 421–428 (2018).MathSciNet 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Tojo, R. et al. Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 20, 15163 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Rodriguez, C. I. & Martiny, J. B. H. Evolutionary relationships among bifidobacteria and their hosts and environments. BMC Genom. 21, 1–12 (2020).Article 

    Google Scholar 
    59.Sharma, V., Mobeen, F. & Prakash, T. Exploration of survival traits, probiotic determinants, host interactions, and functional evolution of bifidobacterial genomes using comparative genomics. Genes 9, 477 (2018).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    60.Sun, Z. et al. Comparative genomic analysis of 45 type strains of the genus Bifidobacterium. a snapshot of its genetic diversity and evolution. PLoS One 10, 0117912 (2015).
    Google Scholar 
    61.Frey, J. C. et al. Fecal bacterial diversity in a wild gorilla. Appl. Environ. Microbiol. 72, 3788–3792 (2006).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Makovska, M., Modrackova, N., Bolechova, P., Drnkova, B. & Neuzil-Bunesova, V. Antibiotic susceptibility screening of primate-associated Clostridium ventriculi. Anaerobe, 102347 (2021).63.Ushida, K. et al. Draft genome sequences of Sarcina ventriculi strains isolated from wild Japanese macaques in Yakushima Island. Genome announcements 4 (2016).64.Owens, L. A. et al. A Sarcina bacterium linked to lethal disease in sanctuary chimpanzees in Sierra Leone. Nat. Commun. 12, 1–16 (2021).ADS 
    Article 
    CAS 

    Google Scholar 
    65.Vlková, E., Rada, V., Šmehilová, M. & Killer, J. Auto-aggregation and co-aggregation ability in bifidobacteria and clostridia. Folia Microbiol. 53, 263–269 (2008).Article 
    CAS 

    Google Scholar 
    66.Wang, L. et al. Adhesive Bifidobacterium induced changes in cecal microbiome alleviated constipation in mice. Front. Microbiol. 10, 1721 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Wei, Y. et al. Protective effects of bifidobacterial strains against toxigenic Clostridium difficile. Front. Microbiol. 9, 888 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    68.Guittar, J., Shade, A. & Litchman, E. Trait-based community assembly and succession of the infant gut microbiome. Nature Commun. 10, 1–11 (2019).Article 
    CAS 

    Google Scholar 
    69.Moore, R. E. & Townsend, S. D. Temporal development of the infant gut microbiome. Open Biol. 9, 190128 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Korpela, K. et al. Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants. Microbiome 6, 1–11 (2018).Article 

    Google Scholar 
    71.Timperio, A. M., Gorrasi, S., Zolla, L. & Fenice, M. Evaluation of MALDI-TOF mass spectrometry and MALDI BioTyper in comparison to 16S rDNA sequencing for the identification of bacteria isolated from Arctic sea water. PloS One 12, 0181860 (2017).Article 
    CAS 

    Google Scholar 
    72.Bäckhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690–703 (2015).PubMed 
    Article 
    CAS 

    Google Scholar 
    73.Brown, C. J. et al. Comparative genomics of Bifidobacterium species isolated from marmosets and humans. Am. J. Primatol. 81, e983 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Killer, J. et al. Gene encoding the CTP synthetase as an appropriate molecular tool for identification and phylogenetic study of the family Bifidobacteriaceae. MicrobiologyOpen 7, e00579 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    75.Milani, C. et al. Evaluation of bifidobacterial community composition in the human gut by means of a targeted amplicon sequencing (ITS) protocol. FEMS Microbiol. Ecol. 90, 493–503 (2014).CAS 
    PubMed 

    Google Scholar 
    76.Srinivasan, R. et al. Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens. PloS One 10, e0117617 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    77.Maiden, M. C. J. et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nature Rev. Microbiol. 11, 728–736 (2013).CAS 
    Article 

    Google Scholar 
    78.Lugli, G. A. et al. Phylogenetic classification of six novel species belonging to the genus Bifidobacterium comprising Bifidobacterium anseris sp. nov., Bifidobacterium criceti sp. nov., Bifidobacterium imperatoris sp. nov., Bifidobacterium italicum sp. nov., Bifidobacterium margollesii sp. nov. and Bifidobacterium parmae sp. nov. Syst. Appl. Microbiol. 41, 173–183 (2018).PubMed 
    Article 

    Google Scholar 
    79.Malukiewicz, J. et al. The effects of host taxon, hybridization, and environment on the gut microbiome of Callithrix marmosets. BioRxiv, 708255 (2019).80.Amato, K. R. et al. Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species. Oecologia 180, 717–733 (2016).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    81.Hernández‐Rodríguez, D., Vásquez‐Aguilar, A. A., Serio‐Silva, J. C., Rebollar, E. A. & Azaola‐Espinosa, A. Molecular detection of Bifidobacterium spp. in faeces of black howler monkeys (Alouatta pigra). J. Med. Primatol. 48, 99–105 (2019).82.Zhu, L. et al. Sex bias in gut microbiome transmission in newly paired marmosets (Callithrix jacchus). Msystems 5, e00910-00919 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Kap, Y. S. et al. Targeted diet modification reduces multiple sclerosis–like disease in adult marmoset monkeys from an outbred colony. J. Immunol. 201, 3229–3243 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Ren, T., Grieneisen, L. E., Alberts, S. C., Archie, E. A. & Wu, M. Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons. Environ. Microbiol. 18, 1312–1325 (2016).PubMed 
    Article 

    Google Scholar 
    85.Xu, B. et al. Metagenomic analysis of the Rhinopithecus bieti fecal microbiome reveals a broad diversity of bacterial and glycoside hydrolase profiles related to lignocellulose degradation. BMC Genom. 16, 1–11 (2015).Article 
    CAS 

    Google Scholar 
    86.Baumann, P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59, 155–189 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Killer, J. et al. Bifidobacterium actinocoloniiforme sp. nov. and Bifidobacterium bohemicum sp. nov., from the bumblebee digestive tract. Int. J. Syst. Evol. Microbiol. 61, 1315–1321 (2011).88.Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    89.Garber, P. A., Mallott, E. K., Porter, L. M. & Gomez, A. The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small‐bodied primate. Am. J. Primatol. 81, e23003 (2019).90.Gralka, M., Szabo, R., Stocker, R. & Cordero, O. X. Trophic interactions and the drivers of microbial community assembly. Curr. Biol. 30, R1176–R1188 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    91.Clayton, J. B. et al. Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Sci. Rep. 8, 1–16 (2018).CAS 
    Article 

    Google Scholar 
    92.Koo, B. S. et al. Idiopathic chronic diarrhea associated with dysbiosis in a captive cynomolgus macaque (Macaca fascicularis). J. Med. Primatol. 49, 56–59 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    93.Krynak, K. L., Burke, D. J., Martin, R. A. & Dennis, P. M. Gut microbiome composition is associated with cardiac disease in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). FEMS Microbiol. Lett. 364 (2017).94.Modrackova, N. et al. Prebiotic potential of natural gums and starch for bifidobacteria of variable origins. Bioact. Carbohydr. Diet. Fibre 20, 100199 (2019).95.McKenzie, V. J., Kueneman, J. G. & Harris, R. N. Probiotics as a tool for disease mitigation in wildlife: insights from food production and medicine. Ann. N. Y. Acad. Sci. 1429, 18–30 (2018).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    96.Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1–18 (2018).CAS 
    Article 

    Google Scholar 
    97.Hungate, R. E. & Macy, J. The roll-tube method for cultivation of strict anaerobes. Bulletins from the ecological research committee, 123–126 (1973).98.Rada, V. & Petr, J. A new selective medium for the isolation of glucose non-fermenting bifidobacteria from hen caeca. J. Microbiol. Methods 43, 127–132 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    99.Orban, J. I. & Patterson, J. A. Modification of the phosphoketolase assay for rapid identification of bifidobacteria. J. Microbiol. Methods 40, 221–224 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    100.Kim, B. J., Kim, H.-Y., Yun, Y.-J., Kim, B.-J. & Kook, Y.-H. Differentiation of Bifidobacterium species using partial RNA polymerase β-subunit (rpoB) gene sequences. Int. J. Syst. Evol. Microbiol. 60, 2697–2704 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    101.Hall, T. A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. 41 edn 95–98 ([London]: Information Retrieval Ltd., c1979-c2000.).102.Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    103.Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    104.Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Ress 41, D590–D596 (2012).Article 
    CAS 

    Google Scholar 
    105.Shannon, C. E. & Weaver, W. The mathematical theory of information. Urbana: University of Illinois Press 97 (1949).106.Pielou, E. C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13, 131–144 (1966).ADS 
    Article 

    Google Scholar 
    107.Mandal, S. et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis. 26, 27663 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    108.fundamental algorithms for scientific computing in Python. Virtanen, P. et al. SciPy 1.0. Nat. Methods 17, 261–272 (2020).Article 
    CAS 

    Google Scholar 
    109.Seabold, S. & Perktold, J. Statsmodels: Econometric and statistical modeling with python in Proceedings of the 9th Python in Science Conference 57 (Austin, TX, 2010).110.MacKinnon, J. G. & White, H. Some heteroskedasticity-consistent covariance matrix estimators with improved finite sample properties. J. Econom. 29, 305–325 (1985).Article 

    Google Scholar  More

  • in

    Population consequences of climate change through effects on functional traits of lentic brown trout in the sub-Arctic

    Sampling and dataThe data consist of gillnet catches of brown trout (N = 5733, caught during 2008–2009) from 21 lakes situated along an altitudinal gradient (30 m above sea level, m.a.s.l.-800 m.a.s.l.) in mid-Norway and Sweden (Fig. 5). The lakes were sampled within three main types of vegetation zonation in the catchment area that ranged from the southern boreal to the alpine zone. The lowland lakes were situated in the southern boreal zone dominated by coniferous woodland and forest, but there were also large areas of alder (Alnus sp.) as well as some broad-leaved deciduous woodland. Average annual and July air temperature are 4–6 and 12–16 °C, respectively46. Middle boreal catchment area is dominated by coniferous woodland, forest and mires. Average annual and July air temperature are, respectively, 2–4 and 8–12°C46. Vegetation around the high altitude lakes were dominated by bilberry (Vaccinium myrtillus), grass heaths and dwarf birch (Betula nana) scrub, with annual and July air temperature of − 2 to 0 and 6–12°C46. The clustering of lakes within vegetations zones can be seen in Fig. 5. The epilimnetic water temperature across a sample of the lakes in the altitudinal gradient in this study seems to be within the general trends in the air temperature47.Figure 5Study lake positions (filled dots) and names. Unfilled large circles connects the different lakes with the most representative weather stations (stars) in the area (in terms of altitude, vegetation zones and landscape). The dashed line constitute the national border between Norway and Sweden. The figure was produced using Adobe illustrator.Full size imageAll lakes were sampled using standardised gillnet series consisting of single mesh nets (25 × 1.5 m) with mesh sizes 12.5, 16, 19.5, 24, 29 and 35 mm47. Three nets were linked together making chains with alternating mesh sizes in order to represent all mesh sizes at different depths in each lake at each sampling. This gillnet series catches brown trout with a slight bias in favour of larger individuals48 that was assumed similar in all lakes. The nets were distributed along the shoreline, and the lakes were fished during summer, with different effort (i.e., number of gillnet series) depending on lake size. Weight per unit catch effort (CPUE) based on total weight of the brown trout catch per 100 m2 gillnet area per night was used as a proxy for biomass density. Since, differences in environmental conditions across lakes cause large variations in body size and hence per capita resource demands, biomass was considered a better measure of population density than number of individuals for among-lake comparisons. Length (total length, mm) and weight (g) at catch were measured for every individual in the full data set. Age, sex, maturation status and back-calculation of length-at-age was undertaken for a randomly selected representative subset (N = 889) of the data. Growth and spawning probability ogives49 were modeled based on this subset. Scale samples and otoliths were taken and used for age determination, of which scales were used primarily, and scales were used for back-calculation of growth50. Distance between the annuli was measured, and a direct proportional relationship between the length of the fish and the scale radius was assumed51. If the scales were difficult to read, which was the case for more slow-growing individuals from the low altitude lakes were the annuli were less distinct, otoliths were used for determining the age. As we did not have complete records of water temperature, area and time specific summer air temperature and precipitation measurements were obtained from an online database (www.eklima.no, Norwegian Metrological Institute). The database contained historical weather data from the closest representative (i.e., corresponding in distance, altitude and operational period) weather stations to the respective lakes (Fig. 5). This resulted in overlapping temperature and precipitation regimes for some of the lakes as there were in total five different weather stations that were most representative within the area containing the 21 lakes. Further, as there was some variation in how complete the different measurements were within years, we also had to calculate the sum of summer precipitation for a shorter period of the summer compared to the average mean air temperature. Both measurements still being good proxies for experienced summer conditions in the bulk of the growth season. The effect of temperature and precipitation was thus derived from the spatio-temporal variation in observations between these five weather stations, where the historic temporal variation corresponds to recorded climate components relevant to years for the back calculated age of the individual fish in the specific lakes (resulting in a total of 29 distinct measurements, see variation in Table 2) Epilimnetic water of lakes usually reflects warming trends in air temperature well, however hypolimnetic temperature variation might not be very correlated to the air temperature. Yet, changes in air temperature might indeed influence the thermal stratification of a lake and thus the environment and conditions for a fish52. There are good reasons to believe that most of the lakes in our study obtained some sort of thermal stratification during the summer season. Nonetheless, we chose not to model air to water temperature for the few measurements of water temperatures we had, and extrapolate this relationship to the full spatio-temporal resolution of the data. The rationale for this was threefold: (1) We were interested in exploring potential effects and relationships of easily available climate components, such as air temperature, simplifying the model concept; (2) we did not have access to detailed data on lake bathymetry so that hypothetical modeled air-to-water relationships would be rather uncertain; (3) we had no detailed information on how the brown trout was distributed in the water column during the summer period in study lakes. However, compared to similar lakes, there are reasons to believe that brown trout mainly feed and stay in the upper six meters of the water column, as well as epibenthic areas with high invertebrate abundances53,54, where both areas often are overlapping and highly influenced by the air temperature.Table 2 Description of candidate variables used in the model selection process determining the most supported model for individual growth of brown trout.Full size tableData analysis and model descriptionsOverall processWe used linear mixed model approaches to parameterize environmental effects on key life history traits for brown trout. Specifically: Length at age was parameterized as function of the environment (e.g., summer temperature, population density, winter NAO and summer precipitation). Spawning probability were modeled as functions of individual length and age. We also allowed either the age effect or length effect on spawning probability to vary with temperature or summer precipitation. Individual fecundity (number of eggs produced) was predicted as a function of length and spawning probability. Annual survival estimates from age 1 and up was accessed using catch curve analysis, while first year survival was estimated based on a stock-recruitment function. The estimated parameters were utilized to feed an age structured matrix projection model23, enabling long-term population viability projections in an changing environment (see overview in Fig. 6). Although there are several choices of population models that might be utilized for inferring the population dynamics, such as IBMs55 and IPMs56, the age structured matrix model was deemed especially suited to model our systems as they are highly seasonal (with very reduced growth during winter) and thus producing a clear age structure in the data. Further description of the various modeling approaches are described below. All statistical analyses was done in R57.Figure 6A schematic overview of the processes involved in our model-setup. Red lines indicate drivers and connections acting on individual life history traits, blue lines indicates traits driving the population model and green lines indicates links to climate variables. In short, existing area and time specific climate data on summer precipitation (Prec) and mean summer air temperature (Temp), as well as time specific data on winter NAO-index (recorded NAO values during December, January, February and March, NAO.DJFM), were used to parameterize models for length at age 1 and length at age  > 1, as well as spawning probability at age. Length at age 1 was allowed to affect length at age  > 1, and in the simulations achieved length at age  > 1 was also influenced by the achieved length the previous year (L*). Length at age and spawning probability, both defined by climate variables, interacted in defining how many eggs a female was likely to produce (i.e. fecundity). Survival from eggs to small juvenile fish was based on a stock-recruitment relationship, where the stock was defined by the results from the population model (expected number of fish). Expected number of fish across all ages was also allowed to affect length at age  > 1. The model parameters was used to simulate long term population dynamics, where we also varied expected temperature change scenarios (steadily increasing mean temperatures and temperature variation, respectively, as well as a combination of the two latter scenarios). The populations long term rate of increase (λ) was inferred using the age structured population matrix model.Full size imageSize at ageData inspections prior to model development showed length at age to be surprisingly linear within the size and age distribution in our data (i.e. no obvious signs of asymptotic growth for fish in any of the sampled lakes). Length (L) was thus explored using a linear mixed effects model approach with the lme4-package58. Denoted, length for individual j in population i (Lij) could thus be expressed as:$${L}_{ij}={sumlimits_{k=1}^{p}}{chi }_{ijk}{beta }_{k}$$Here, β = (β1, …, βp)T is px1 vector (one column matrix) of unknown regression parameters, χiT = (χi1, …, χip) ∈ ℝp is the explanatory variables of interest (k + p  1, age was always included as a variable, and we also tested models including an effect of CPUE and first year growth on subsequent growth trajectories. Multiple candidate models where the different environmental effects were allowed to vary with age were constructed (Supplementary information S1). Population ID and individual ID were included as nested random effects in all candidate models exploring size at age  > 1, and population ID was included as a random effect for the models exploring size at age 1. The most supported models were selected based on AIC-values59. During the population simulation the variation in the predictions attributed to the random effect(s) was treated as random noise, and not explicitly included in the simulations.Spawning probabilityBrown trout is an iteroparous species, however under normal food conditions and harsh winters in Norway it might not spawn every year following maturity. Accordingly, we modelled likelihood of spawning at age, derived from the number of female individuals that was going to spawn the following autumn, rather than probability of maturation at age. Aging effects on spawning probability was included in the modelling as skipped-spawning individuals (i.e., mature females that skip spawning episodes, sensu Rideout and Tomkiewicz 60) were coded as non-spawners in the analysis. Probability of spawning (P) was calculated based on a maturation-ogives approach61, utilizing generalized linear mixed effects models in the lme4-package58. Binomial models as two-dimensional ogives, o(A, L) were considered in the model selection. Here, A and L represent age and length, respectively. In addition, we also explored how these ogives might change due to either a temperature effect, summer precipitation effect, or a measure of fish abundance (CPUE) including either as an additive effect in some candidate models (see Supplementary information S2). Population ID was always included as a random effect. In general, the probability of spawning could thus be described as:$${mathrm{Pr}left(spawningright)}_{ij}={beta }_{0i}+{beta }_{1i}{A}_{ij}+{beta }_{2i}{L}_{ij}+{beta }_{3i}{A}_{ij}{L}_{ij}+{beta }_{4i}{x}_{1i}+{a}_{i}+{varepsilon }_{ij}$$
    where βs represent coefficients under estimation, Aij = age of individual j in population i, L = individual length, x1 represent a lake-specific environmental variable (if present in the candidate model, either summer temperature, CPUE or precipitation), ai is the estimated random lake-specific intercept and εij is the random residual variation assumed normally distributed on logit scale. The most supported model was selected based on AICc-values59.FecundityFemale fecundity (i.e., number of eggs per female) was predicted as a function of female length (mm) and two constants based upon published values for brown trout from Norway (F = e log(l)*2.21–6.15)62 multiplied by the probability of spawning (P) at size and age.SurvivalAnnual survival rates (s) for fish age ≥ 1 were based on estimations from catch-curve slopes utilizing the Chapman-Robson function in the FSA-package63. The survival was estimated based on descending catch curves, i.e., where numbers of caught individuals decreased as a function of age in the catch. Based on this slope we can derive an instantaneous mortality rate (Z), and from this the annual survival rate could be estimated from S = e-Z. Due to a restricted number of populations available for survival rates, the survival was estimated across all population. As it is unlikely that S would be constant across all age classes we choose to make age specific survival rates, Sa, where the S1 (survival from age one to age two) was reduced, and S3-5 was slightly increased whereas all other Sa = S. The respective reduction and increase are described more in detail below. Survival rates for age 0–1, S0, was based on a stock-recruitment function (see further description under “Climate scenarios, calibration and population projections”).The projection matrixPopulation projections were derived utilizing an age-structured matrix population model23 in the popbio-package in R64. Changes in the age structure and abundance of brown trout was modelled from Nt+1 = K(E,N,t)Nt or rather:$${left[begin{array}{c}{N}_{1}\ {N}_{2}\ vdots \ vdots \ {N}_{{a}_{max}}end{array}right]}_{t+1}=left[begin{array}{ccccc}{f}_{1}left(L,P,{N}_{t}right){s}_{0}left({E}_{t}right)& {f}_{2}left(L,P,{N}_{t}right){s}_{0}left({E}_{t}right)& cdots & cdots & {f}_{{a}_{max}}left(L,P,{N}_{t}right){s}_{0}left({E}_{t}right)\ {s}_{a}& 0& cdots & cdots & 0\ 0& {s}_{a}& cdots & cdots & 0\ vdots & vdots & vdots & vdots & vdots \ 0& 0& 0& {s}_{a}& 0end{array}right]times {left[begin{array}{c}{N}_{1}\ {N}_{2}\ vdots \ vdots \ {N}_{{a}_{max}}end{array}right]}_{t}$$
    where Nt is the abundance of brown trout across all age classes a = 1,…, amax at year t. Census time is chosen so that reproduction occurs at the beginning of each annual season. fa is the fecundity at age a (i.e., the number of offspring produced per individual of age a during a year). More specifically, f varies according to f(L,P,N), where variations in L (length) and P (probability to spawn) in turn is defined by climate variables and the number of individuals N. s is a constant and represent the survival probability of individuals from age a to age a + 1, and amax is the maximum age considered in the model. amax was set to 10 years in the simulations, as was also was the age of the oldest fish in the aged subset of the data (see frequency table in Supplementary information S2). Although varying between systems, the maximum age observed and simulated also corresponds to expected maximum age found in other systems in Norway65. S0 is a function of E, the numbers of eggs laid, where the relationship is determined by a stock-recruitment function.Consequently, K(E,N,t), the Leslie matrix, is a function of N and E. In each time step, the survival of individuals in age class amax is 0, whereas individuals at all other ages spawn and experience mortality as defined above. From the Leslie matrix K, we can infer the population’s long-term rate of increase, λ, from the dominant eigenvector of the matrix23.Climate scenarios, calibration and population projectionsTo explore the population effects of changes in summer air temperature or winter conditions we simulated different 100-years climate-change scenarios for a single lake, which included variations the climate variables in focus. The first scenario represented a status quo setting. Here, annual average summer air temperatures were randomly drawn from a normal distribution with mean and standard deviation from observed summer air temperatures from 1998–2009 in the study area. The second climate scenario randomly assigned temperatures as in scenario one, as well as allowing for more and more fluctuating annual summer temperatures as time progressed. This was done by adding a random variable t (~ N(0,0.03) times the number of the specific year (i.e., 1–100) in the 100-years climate change scenario. The third climate scenario, drew annual summer temperatures as in the first scenario, but included an increase in the average air summer temperature by 0.04 °C each year (i.e., 4 °C in total for the 100-year-scenario which is close to the expected mean increase in regional temperature following the regionally down-scaled RCP8.5 IPCC scenario66). The fourth climate scenario included an average summer temperature increase of 0.02 °C each year (close to the expected average temperature increase following the regionally down-scaled RCP4.5 IPCC scenario66), as well as allowing for more and more fluctuating annual summer temperatures as time progressed (as in scenario two). For all climate scenarios above, annual winter NAO-values was randomly drawn from a uniform distribution between − 1.5 and 1.5.We also simulated a second set of climate change scenarios, where summer temperatures were as described in the four scenarios above, however in all these scenarios we also included a trend of higher winter NAO values (meaning a general trend of warmer winters with more precipitation/snow in the study area, as predicted by the down scaled climate scenarios66). This was done by letting annual NAO-values be drawn from a random normal distribution with mean = 0.5, and standard deviation of 0.5.During the calibration process for the simulations, we altered the age specific survival estimates S1 and S3-5 so that average lambdas for the status quo climate scenario was relatively stable and close to 1 (i.e. no large changes in population size) based on 100 iterations of a 100 year-climate scenario. Specifically, S1 = S*0.6 and S3-5 = S*1.2, which is also assumed to be within the realistic range of survival rates for the specific age classes in the focal populations. S0 was derived from a stock recruitment function, and was thus allowed to vary as a function of density in the population. Specifically, from the total egg number (Et) at year t and the number of one-year olds at year t + 1 (N1,t+1) the stock-recruitment function could be estimated by fitting a Shepherd function67:$${N}_{1,t+1}=frac{a{E}_{t}}{{left(1+b{E}_{t}right)}^{c}}$$
    where a = 0.04, b = 0.0000003 and c = 3.5. E is number of eggs deposited during t-1 spawning season, estimated as the total fecundity. The estimated N1,t+1 was used to estimate first-year survival (s0) from:$${s}_{0,t}=mathrm{ln}left({E}_{t-1}right)-mathrm{ln}left({N}_{1,t}right)$$All 100-years scenarios were simulated with 100 iterations to extract the variation in the expected population projections. CPUE in the simulations was included as a dynamic variable in the growth model, recalculated through the matrix projection model for each time step, i.e. year. Length at age, spawning probability and fecundity was predicted for each time step (i.e. pr year) as described above. The spawning probability did however not vary annually according to changes in the environment but was predicted according to the mean values of the environmental variables across all years the climate scenario. However, for climate scenarios with increasing mean temperature over time, the expected spawning probability was a function of the gradual mean temperature increase. Thus, by allowing the spawning probability reaction norm gradually to follow changes in the temperature, as predicted from the spawning model, we allowed the populations to gradually adapt the reaction norm to the respective changes. More

  • in

    Comparative assessment of amino acids composition in two types of marine fish silage

    Degree of hydrolysisOrganic silages prepared from fat fish (FFS) and lean fish (LFS) had a characteristic tawny brown colour which was accompanied with a strong characteristic salty-fishy odour. At the end of 5 DoF, both FFS and LFS exhibited sluggish liquefaction which increased progressively concomitant with the DoF (Table S1). Liquefaction is an indicator of tissue hydrolysis due to the action of acid. During 35 DoF, the degree of hydrolysis (measured in terms of liquefaction volume) increased progressively with the DoF in both types of ensilages and was relatively higher in LFS compared to FFS on all sampled DoF (Table S1). In general, lipolysis supersedes the proteolysis in all major biochemical processes23. A relatively higher degree of hydrolysis recorded in LFS may be attributed to the presence of a greater proportion of light muscles compared to dark muscles. Relatively greater susceptibility of light muscles to hydrolysis compared to dark muscles might be due to lower lipid content in the former23.Irrespective of fish type, the measured pH values in both types of ensilages (FFS and LFS) were similar (data not shown) and the values showed a progressive increase from 1.0 ± 0.03 (0 DoF) to 6.0 ± 0.03 (35 DoF). Such an increasing trend in pH with the advancement in DoF could be attributable to gradual solubilisation of boney material with the advancement fermentation time24,25,26.Changes in principal biochemical constituentsDuring the 35 DoF, the concentrations of total protein (TP) in both FFS and LFS progressively increased with the DoF and showed significant differences with the advancement of DoF (p  phenylalanine (2.6 ± 0.033)  > serine (2.4 ± 0.033)  > aspartic acid (2.3 ± 0.033)  > alanine (2.1 ± 0.033)  > histidine (1.8 ± 0.033)  > valine (1.6 ± 0.033)  > methionine (1.5 ± 0.033)  > isoleucine (1.5 ± 0.033)  > threonine (1.4 ± 0.033)  > cysteine (0.946 ± 0.033).Figure 1Composition of total amino acids (mg/g) in two types of fish ensilages (FFS—fat fish silage; LFS—lean fish silage) during 35 days of fermentation (DoF). Data are mean ± SD. * p  glutamic acid (4.97 ± 0.033)  > arginine (4.5 ± 0.033)  > phenylalanine (3.38 ± 0.033)  > aspartic acid (2.92 ± 0.033)  > alanine (2.23 ± 0.033)  > methionine (2.19 ± 0.033)  > lysine (1.882 ± 0.033)  > serine (1.881 ± 0.033)  > tyrosine (1.410 ± 0.033)  > glycine (1.219 ± 0.033)  > threonine (0.953 ± 0.033)  > valine (0.945 ± 0.033)  > isoleucine (0.864 ± 0.033)  > histidine (0.417 ± 0.033).A comparative assessment of profiles of TAA in both FSS and LFS during all DoF revealed a similar pattern, albeit with obvious differences in the concentration of few amino acids (Fig. 1). It has been hypothesised that the occurrence of decarboxylation that follows transamination of amino acids as a consequence of increase in pH during fermentation is known to cause a decrement in the concentration of few amino acids, especially valine and isoleucine34. During the present study, the concentrations of histidine, valine, isoleucine, glycine and lysine were significantly higher (p  leucine (3.09 ± 0.003)  > glutamic acid (2.61 ± 0.003)  > alanine (1.83 ± 0.003)  > phenylalanine (1.79 ± 0.003)  > cysteine (1.67 ± 0.003)  > histidine (1.56 ± 0.003)  > aspartic acid (1.54 ± 0.003)  > serine (1.32 ± 0.003)  > lysine (1.16 ± 0.003)  > threonine (1.09 ± 0.003)  > valine (1.07 ± 0.003)  > isoleucine (1.06 ± 0.003) followed by methionine (0.93 ± 0.003)  > tyrosine (0.92 ± 0.003)  > tryptophan (0.72 ± 0.003)  > asparagine (0.57 ± 0.003)  > glutamine (0.15 ± 0.003).Figure 2Composition of free amino acids (mg/g) in two types of fish ensilages (FFS—fat fish silage; LFS—lean fish silage) during 35 days of fermentation (DoF). Data are mean ± SD. * p  More

  • in

    Early life neonicotinoid exposure results in proximal benefits and ultimate carryover effects

    1.Mineau, P. & Palmer, C. Neonicotinoid Insecticides and Birds: The Impact of the Nation’s Most Widely Used Insecticides on Birds. (American Bird Conservancy, USA, 2013).2.Simon-Delso, N. et al. Systemic insecticides (Neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environ. Sci. Pollut. Res. 22, 5–34. https://doi.org/10.1007/s11356-014-3470-y (2015).CAS 
    Article 

    Google Scholar 
    3.Jeschke, P., Nauen, R., Schindler, M. & Elbert, A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 59, 2897–2908. https://doi.org/10.1021/jf101303g (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Tomizawa, M. & Casida, J. E. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotining receptors. Annu. Rev. Entomol. 48, 339–364. https://doi.org/10.1146/annurev.ento.48.091801.112731 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    5.Woodcock, B. A. et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 1–8. https://doi.org/10.1038/ncomms12459 (2016).CAS 
    Article 

    Google Scholar 
    6.Pisa, L. et al. An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: Impacts on organisms and ecosystems. Environ. Sci. Pollut. Res. 28, 1–49. https://doi.org/10.1007/s11356-017-0341-3 (2017).CAS 
    Article 

    Google Scholar 
    7.Li, Y., Miao, R. & Khanna, M. Neonicotinoids and decline in bird biodiversity in the United States. Nat. Sustain. 3, 1027–1035. https://doi.org/10.1038/s41893-020-0582-x (2020).Article 

    Google Scholar 
    8.Eng, M. L., Stutchbury, B. J. & Morrissey, C. A. Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Sci. Rep. 7, 1. https://doi.org/10.1038/s41598-017-15446-x (2017).CAS 
    Article 

    Google Scholar 
    9.Eng, M. L., Stutchbury, B. J. & Morrissey, C. A. A neonicotinoid insecticide reduces fueling and delays migration in songbirds. Science 80(365), 1177–1180. https://doi.org/10.1126/science.aaw9419 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Lopez-Antia, A., Ortiz-Santaliestra, M. E., Mougeot, F. & Mateo, R. Imidacloprid-treated seed ingestion has lethal effect on adult partridges and reduces both breeding investment and offspring immunity. Environ. Res. 136, 97–107. https://doi.org/10.1016/j.envres.2014.10.023 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Pandey, S. P. & Mohanty, B. The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide mancozeb disrupt the pituitary-thyroid axis of a wildlife bird. Chemosphere 122, 227–234. https://doi.org/10.1016/j.chemosphere.2014.11.061 (2015).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    12.Tokumoto, J. et al. Effects of exposure to clothianidin on the reproductive system of male quails. J. Vet. Med. Sci. 75, 755–760. https://doi.org/10.1292/jvms.12-0544 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Addy-Orduna, L. M., Brodeur, J. C. & Mateo, R. Oral acute toxicity of imidacloprid, thiamethoxam and clothianidin in eared doves: A contribution for the risk assessment of neonicotinoids in birds. Sci. Total Environ. 650, 1216–1223. https://doi.org/10.1016/j.scitotenv.2018.09.112 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Berheim, E. H. et al. Effects of Neonicotinoid Insecticides on Physiology and Reproductive Characteristics of Captive Female and Fawn White-tailed Deer. Sci. Rep. 9, 1–10. https://doi.org/10.1038/s41598-019-40994-9 (2019).CAS 
    Article 

    Google Scholar 
    15.Wang, Y. et al. Unraveling the toxic effects of neonicotinoid insecticides on the thyroid endocrine system of lizards. Environ. Pollut. 258, 113731. https://doi.org/10.1016/j.envpol.2019.113731 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    16.Khalil, S. R., Awad, A., Mohammed, H. H. & Nassan, M. A. Imidacloprid insecticide exposure induces stress and disrupts glucose homeostasis in male rats. Environ. Toxicol. Pharmacol. 55, 165–174. https://doi.org/10.1016/j.etap.2017.08.017 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    17.Abou-Donia, M. B. et al. Imidacloprid induces neurobehavioral deficits and increases expression of glial fibrillary acidic protein in the motor cortex and hippocampus in offspring rats following in utero exposure. J. Toxicol. Environ. Heal. – Part A Curr. Issues 71, 119–130. https://doi.org/10.1080/15287390701613140 (2008).CAS 
    Article 

    Google Scholar 
    18.Gawade, L., Dadarkar, S. S., Husain, R. & Gatne, M. A detailed study of developmental immunotoxicity of imidacloprid in Wistar rats. Food Chem. Toxicol. 51, 61–70. https://doi.org/10.1016/j.fct.2012.09.009 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    19.Mohanty, B., Pandey, S. P. & Tsutsui, K. Thyroid disrupting pesticides impair the hypothalamic-pituitary-testicular axis of a wildlife bird. Amandava amandava. Reprod. Toxicol. 71, 32–41. https://doi.org/10.1016/j.reprotox.2017.04.006 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Sun, Q. et al. Imidacloprid Promotes High Fat Diet-Induced Adiposity in Female C57BL/6J Mice and Enhances Adipogenesis in 3T3-L1 Adipocytes via the AMPK(alpha)-Mediated Pathway. J. Agric. Food Chem. 65, 6572–6581. https://doi.org/10.1021/acs.jafc.7b02584 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Sun, Q. et al. Imidacloprid promotes high fat diet-induced adiposity and insulin resistance in male C57BL/6J mice. J. Agric. Food Chem. 64, 9293–9306. https://doi.org/10.1021/acs.jafc.6b04322 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Park, Y. et al. Imidacloprid, a neonicotinoid insecticide, potentiates adipogenesis in 3T3-L1 adipocytes. J. Agric. Food Chem. 61, 255–259. https://doi.org/10.1021/jf3039814 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    23.Ricklefs, R. E., Stark, J. M. & Konarzewski, M. Internal constraints on growth in birds. in Avian Growth and Development. Evolution within the Altricial-Precocial Spectrum (eds Starck, J. M. & Ricklefs, R.E.) 266–287 (Oxford Ornithology Series, Oxford, 1998).
    Google Scholar 
    24.Bobek, S., Jastrzebski, M. & Pietras, M. Age-related changes in oxygen consumption and plasma thyroid hormone concentration in the young chicken. Gen. Comput. Endocrinol. 31, 169–174. https://doi.org/10.1016/0016-6480(77)90014-4 (1977).CAS 
    Article 

    Google Scholar 
    25.Metcalfe, N. B. & Monaghan, P. Compensation for a bad start: Grow now, pay later?. Trends Ecol. Evol. 16, 254–260. https://doi.org/10.1016/S0169-5347(01)02124-3 (2001).Article 
    PubMed 

    Google Scholar 
    26.Criscuolo, F., Monaghan, P., Nasir, L. & Metcalfe, N. B. Early nutrition and phenotypic development: “catch-up” growth leads to elevated metabolic rate in adulthood. Proc. Biol. Sci. 275(1642), 1565–1570. https://doi.org/10.1098/rspb.2008.0148 (2008).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Monaghan, P. Early growth conditions, phenotypic development and environmental change. Philos. Trans. R. Soc. B Biol. Sci. 363, 1635–1645. https://doi.org/10.1098/rstb.2007.0011 (2008).Article 

    Google Scholar 
    28.Lee, W. S., Monaghan, P. & Metcalfe, N. B. The pattern of early growth trajectories affects adult breeding performance. Ecology 93, 902–912. https://doi.org/10.1890/11-0890.1 (2012).Article 
    PubMed 

    Google Scholar 
    29.Zera, A. J. & Harshman, L. G. The Physiology of Life History Trade-Offs in Animals. Annu. Rev. Ecol. Syst. 32, 95–126. https://doi.org/10.1146/annurev.ecolsys.32.081501.114006 (2001).Article 

    Google Scholar 
    30.Botías, C., David, A., Hill, E. M. & Goulson, D. Quantifying exposure of wild bumblebees to mixtures of agrochemicals in agricultural and urban landscapes. Environ. Pollut. 222, 73–82. https://doi.org/10.1016/j.envpol.2017.01.001 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Hladik, M. L. & Kolpin, D. W. First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA. Environ. Chem. 13, 12. https://doi.org/10.1071/EN15061 (2016).CAS 
    Article 

    Google Scholar 
    32.Morrissey, C. A. et al. Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: A review. Environ. Int. 74, 291–303. https://doi.org/10.1016/j.envint.2014.10.024 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    33.McNabb, F. M. A. The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit. Rev. Toxicol. 37(1–2), 163–193. https://doi.org/10.1080/10408440601123552 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    34.Gobeli, A., Crossley, D., Johnson, J. & Reyna, K. The effects of neonicotinoid exposure on embryonic development and organ mass in northern bobwhite quail (Colinus virginianus). Comp. Biochem. Physiol. Part – C Toxicol. Pharmacol. 195, 9–15. https://doi.org/10.1016/j.cbpc.2017.02.001 (2017).CAS 
    Article 

    Google Scholar 
    35.Mineau, P. & Callaghan, C. Neonicotinoid insecticides and bats: an assessment of the direct and indirect risks. (Canadian Wildlife Federation, 2018).36.Wilson, J. D., Morris, A. J., Arroyo, B. E., Clark, S. C. & Bradbury, R. B. A review of the abundance and diversity of invertebrate and plant foods of granivorous birds in northern Europe in relation to agricultural change. Agric. Ecosyst. Environ. 75, 13–30. https://doi.org/10.1016/S0167-8809(99)00064-X (1999).Article 

    Google Scholar 
    37.Peig, J. & Green, A. J. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 1883–1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x (2009).Article 

    Google Scholar 
    38.Spencer, K., Buchanan, K., Goldsmith, A. & Catchpole, C. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44, 132–139. https://doi.org/10.1016/S0018-506X(03)00124-7 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Ayyanath, M.-M., Cutler, G. C., Scott-Dupree, C. D. & Sibley, P. K. Transgenerational Shifts in Reproduction Hormesis in Green Peach Aphid Exposed to Low Concentrations of Imidacloprid. PLoS One 8, e74532. https://doi.org/10.1371/journal.pone.0074532 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    40.Calabrese, E. J. & Baldwin, L. A. Toxicology rethinks its central belief. Nature 421, 691–692. https://doi.org/10.1038/421691a (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    41.Lopez-Antia, A., Ortiz-Santaliestra, M. E., Mougeot, F. & Mateo, R. Experimental exposure of red-legged partridges (Alectoris rufa) to seeds coated with imidacloprid, thiram and difenoconazole. Ecotoxicology 22, 125–138. https://doi.org/10.1007/s10646-012-1009-x (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    42.Rix, R. R., Ayyanath, M. M. & Christopher Cutler, G. Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J. Pest Sci. (2004) 89, 581–589. https://doi.org/10.1007/s10340-015-0716-5 (2016).Article 

    Google Scholar 
    43.von Engelhardt, N. & Groothuis, T. G. G. Maternal hormones in avian eggs. in Hormones and Reproduction of Vertebrates: Birds, 1st edn. (eds Norris, D. & Lopez, K.) 91–127. https://doi.org/10.1016/C2009-0-01697-3 (Academic Press, 2011).Chapter 

    Google Scholar 
    44.Hulbert, A. J. Thyroid hormones and their effects: A new perspective. Biol. Rev. Camb. Philos. Soc. 75, 519–631. https://doi.org/10.1017/s146479310000556x (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    45.Darras, V. M. et al. Partial Food Restriction Increases Hepatic Inner Ring Deiodinating Activity in the Chicken and the Rat. Gen. Comp. Endocrinol. 100, 334–338. https://doi.org/10.1006/gcen.1995.1164 (1995).CAS 
    Article 
    PubMed 

    Google Scholar 
    46.Klandorf, H. & Harvey, S. Food intake regulation of circulating thyroid hormones in domestic fowl. Gen. Comp. Endocrinol. 60, 162–170. https://doi.org/10.1016/0016-6480(85)90310-7 (1985).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Reyns, G. E., Janssens, K. A., Buyse, J., Kühn, E. R. & Darras, V. M. Changes in thyroid hormone levels in chicken liver during fasting and refeeding. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 132(1), 239–245. https://doi.org/10.1016/s1096-4959(01)00528-0.CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Harvey, S. & Klandorf, H. Reduced adrenocortical function and increased thyroid function in fasted and refed chickens. J. Endocrinol. 98, 129–135. https://doi.org/10.1677/joe.0.0980129 (1983).CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Rimbach, R., Pillay, N. & Schradin, C. Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases. J. Exp. Biol. 220, 837–843. https://doi.org/10.1242/jeb.151449 (2017).Article 
    PubMed 

    Google Scholar 
    50.Scott, I. & Evans, P. R. The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: Implications for BMR/body mass relationships. Comp. Biochem. Physiol. Comp. Physiol. 103(2), 329–332. https://doi.org/10.1016/0300-9629(92)90589-I (1992).CAS 
    Article 
    PubMed 

    Google Scholar 
    51.Mesnage, R., Biserni, M., Genkova, D., Wesolowski, L. & Antoniou, M. N. Evaluation of neonicotinoid insecticides for oestrogenic, thyroidogenic and adipogenic activity reveals imidacloprid causes lipid accumulation. J. Appl. Toxicol. 38, 1483–1491. https://doi.org/10.1002/jat.3651 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Lindström, J. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14(9), 343–348. https://doi.org/10.1016/S0169-5347(99)01639-0 (1999).Article 
    PubMed 

    Google Scholar 
    53.Vézina, F., Love, O. P., Lessard, M. & Williams, T. D. Shifts in metabolic demands in growing altricial nestlings illustrate context-specific relationships between basal metabolic rate and body composition. Physiol. Biochem. Zool. 82, 248–257. https://doi.org/10.1086/597548 (2009).Article 
    PubMed 

    Google Scholar 
    54.Swanson, D. L., Mckechnie, A. E. & Vézina, F. How low can you go ? An adaptive energetic framew ork for interpreting basal metabolic rate variation in endotherms. J. Comp. Physiol. B 187, 1039–1056. https://doi.org/10.1007/s00360-017-1096-3 (2017).Article 
    PubMed 

    Google Scholar 
    55.Hao, C., Eng, M. L., Sun, F. & Morrissey, C. A. Part-per-trillion LC-MS/MS determination of neonicotinoids in small volumes of songbird plasma. Sci. Total Environ. 644, 1080–1087. https://doi.org/10.1016/j.scitotenv.2018.06.317 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    56.Taliansky-Chamudis, A., Gómez-Ramírez, P., León-Ortega, M. & García-Fernández, A. J. Validation of a QuECheRS method for analysis of neonicotinoids in small volumes of blood and assessment of exposure in Eurasian eagle owl (Bubo bubo) nestlings. Sci. Total Environ. 595, 93–100. https://doi.org/10.1016/j.scitotenv.2017.03.246 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    57.Lemon, W. C. The energetics of lifetime reproductive success in the zebra finch Taeniopygia guttata. Physiol. Zool. 66, 946–963. https://doi.org/10.1086/physzool.66.6.30163748 (1993).Article 

    Google Scholar 
    58.Chastel, O., Lacroix, A. & Kersten, M. Pre-breeding energy requirements: thyroid hormone, metabolism and the timing of reproduction in house sparrows (Passer domesticus). J. Avian Biol. 34, 298–306. https://doi.org/10.1034/j.1600-048X.2003.02528.x (2003).Article 

    Google Scholar 
    59.Hicks, O. et al. The role of parasitism in the energy management of a free-ranging bird. J. Exp. Biol. 221(24), jeb190066. https://doi.org/10.1242/jeb.190066 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Guglielmo, C. G., McGuire, L. P., Gerson, A. R. & Seewagen, C. L. Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J. Ornithol. 152, 75–85. https://doi.org/10.1007/s10336-011-0724-z (2011).Article 

    Google Scholar 
    61.Le Pogam, A. et al. Wintering snow buntings elevate cold hardiness to extreme levels but show no changes in maintenance costs. Physiol. Biochem. Zool. 93, 417–433. https://doi.org/10.1086/711370 (2020).Article 
    PubMed 

    Google Scholar 
    62.Lighton, J. R. B. Measuring Metabolic Rates, 2nd edn. https://doi.org/10.1093/oso/9780198830399.001.0001 (Oxford University Press, Oxford, 2018).Book 

    Google Scholar 
    63.Gessaman, J. A. & Nagy, K. A. Energy metabolism: Errors in gas-exchange conversion factors. Physiol. Zool. 61, 507–513. https://doi.org/10.1086/physzool.61.6.30156159 (1988).Article 

    Google Scholar 
    64.R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical  Computing, Vienna, Austria, 2017).65.Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x (2010).Article 

    Google Scholar  More

  • in

    Data sharing practices and data availability upon request differ across scientific disciplines

    Our study uniquely points to differences among scientific disciplines in data availability as published along with the article and upon request from the authors. We demonstrate that in several disciplines such as forestry, materials for energy and catalysis and psychology, critical data are still unavailable for re-analysis or meta-analysis for more than half of the papers published in Nature and Science in the last decade. These overall figures roughly match those reported for other journals in various research fields8,11,13,22, but exceed the lowest reported values of around 10% available data13,23,24. Fortunately, data availability tends to improve, albeit slowly, in nearly all disciplines (Figs. 3, 7), which confirms recent implications from psychological and ecological journals13,31. Furthermore, the reverse trend we observed in microbiology corroborates the declining metagenomics sequence data availability22. Typically, such large DNA sequence data sets are used to publish tens of articles over many years by the teams producing these data; hence releasing both raw data and datasets may jeopardise their expectations of priority publishing. The weak discipline-specific differences among Nature and Science (Fig. 2) may be related to how certain subject editors implemented and enforced stringent data sharing policies.After rigorous attempts to contact the authors, data availability increased by one third on average across disciplines, with full and at least partial availability reaching 70% and 83%, respectively. These figures are in the top end of studies conducted thus far8,22 and indicate the relatively superior overall data availability in Science and Nature compared with other journals. However, the relative rates of data retrieval upon request, decline sharing data and ignoring the requests were on par with studies covering other journals and specific research fields10,12,25,26,28. Across 20 years, we identified the overall loss of data at an estimated rate of 3.5% and 5.9% for initially available data and data effectively available upon request, respectively. This rate of data decay is much less than 17% year−1 previously reported in plant and animal sciences based on a comparable approach24.While the majority of data are eventually available, it is alarming that less than a half of the data clearly stated to be available upon request could be effectively obtained from the authors. Although there may be objective reasons such as force majeure, these results suggest that many authors declaring data availability upon contacting may have abused the publishers’ or funders’ policy that allows statements of data availability upon request as the only means of data sharing. We find that this infringes research ethics and disables fair competition among research groups. Researchers hiding their own data may be in a power position compared with fair players in situations of big data analysis, when they can access all data (including their own), while others have more limited opportunities. Data sharing is also important for securing a possibility to re-analyse and re-interpret unexpected results9,32 and detect scientific misconduct25,33. More rigorous control of data release would prevent manuscripts with serious issues in sampling design or analytical procedures from being prepared, reviewed and eventually accepted for publication.Our study uniquely recorded the authors’ concerns and specific requests when negotiating data sharing. Concerns and hesitations about data sharing are understandable because of potential drawbacks and misunderstandings related to data interpretation and priority of publishing17,34 that may outweigh the benefits of recognition and passive participation in broader meta-studies. Nearly one quarter of researchers expressed various concerns or had specific requests depending on the discipline, especially about the specific objectives of our study. Previous studies with questionnaires about hypothetical data sharing unrelated to actual data sharing reveal that financial interests, priority of additional publishing and fear of challenging the interpretations after data re-analysis constitute the authors’ major concerns12,35,36. Another study indicated that two thirds of researchers sharing biomedical data expected to be invited as co-authors upon use of their data37 although this does not fulfil the authorship criteria6,38. At least partly related to these issues, the reasons for declining data sharing differed among disciplines: while social scientists usually referred to the loss of data, psychologists most commonly pointed out ethical/legal issues. Recently published data were, however, more commonly declined due to ethical/legal issues, which indicates rising concerns about data protection and potential misuse. Although we offered a possibility to share anonymised data sets, such trimmed data sets were never obtained from the authors, suggesting that ethical issues were not the only reason for data decline. Because research fields strongly differed in the frequency of no response to data requests, most unanswered requests can be considered declines that avoid official replies, which may harm the authors’ reputation.Because we did not sample randomly across journals, our interpretations are limited to the journals Nature and Science. Our study across disciplines did not account for the particular academic editor, which may have partly contributed to the differences among research fields and journals. Not all combinations of disciplines, journals and time periods received the intended 25 replicate articles because of the poor representation of certain research fields in the 2000–2009 period. This may have reduced our ability to detect statistically significant differences among the disciplines. We also obtained estimates for the final data availability for seven out of nine disciplines. Although we excluded the remaining two disciplines from comparisons of initial and final data availability, it may have slightly altered the overall estimates. The process of screening the potentially relevant articles chronologically backwards resulted in overrepresentation of more recent articles in certain relatively popular disciplines, which may have biased comparisons across disciplines. However, the paucity of residual year effect and year x discipline interaction in overall models and residual time effect in separate analyses within research fields indicate a minimal bias (Figure S1).We recorded the concerns and requests of authors that had issues with initial data sharing. Therefore, these responses may be relatively more sceptic than the opinions of the majority of the scientific community publishing in these journals. It is likely that the authors who did not respond may have concerns and reasons for declining similar to those who refused data sharing.Our experience shows that receiving data typically required long email exchanges with the authors, contacting other referred authors or sending a reminder. Obtaining data took on average 15 days, representing a substantial effort to both parties39. This could have been easily avoided by releasing data upon article acceptance. On the other hand, we received tips for analysis, caution against potential pitfalls and the authors’ informed consent upon contacting. According to our experience, more than two thirds of the authors need to be contacted for retrieving important metadata, variance estimates or specifying methods for meta-analyses40. Thus, contacting the authors may be commonly required to fill gaps in the data, but such extra specifications are easier to provide compared with searching and converting old datasets into a universally understandable format.Due to various concerns and tedious data re-formatting and uploading, the authors should be better motivated for data sharing41. Data formatting and releasing certainly benefits from clear instructions and support from funders, institutions and publishers. In certain cases, public recognition such as badges of open data for articles following the best data sharing practices and increasing numbers of citations may promote data release by an order of magnitude42. Citable data papers are certainly another way forward43,44, because these provide access to a well-organised dataset and add to the authors’ publication record. Encouraging enlisting published data sets with download and citation metrics in grant and job applications alongside with other bibliometric indicators should promote data sharing. Relating released data in publicly available research accounts such as ORCID, ResearcherID and Google Scholar would benefit both authors, other researchers and evaluators. To account for many authors’ fear of data theft17 and to prioritise the publishing options of data owners, setting a reasonable embargo period for third-party publishing may be needed in specific cases such as immediate data release following data generation45 and dissertations.All funders, research institutions, researchers, editors and publishers should collectively contribute to turn data sharing into a win-win situation for all parties and the scientific endeavour in general. Funding agencies may have a key role here due to the lack of conflicting interests and a possibility of exclusive allocation to depositing and publishing huge data files46. Funders have efficient enforcing mechanisms during reports periods, with an option to refuse extensions or approving forthcoming grant applications. We advocate that funders should include published data sets, if relevant, as an evaluation criterion besides other bibliometric information. Research institutions may follow the same principles when issuing institutional grants and employing research staff. Institutions should also insist their employees on following open data policies45.Academic publishers also have a major role in shaping data sharing policies. Although deposition and maintenance of data incur extra costs to commercial publishers, they should promote data deposition in their servers or public repositories. An option is to hire specific data editors for evaluating data availability in supplementary materials or online repositories and refusing final publishing before the data are fully available in a relevant format47. For efficient handling, clear instructions and a machine-readable data availability statement option (with a QR code or link to the data) should be provided. In non-open access journals, the data should be accessible free of charge or at reduced price to unsubscribed users. Creating specific data journals or ‘data paper’ formats may promote publishing and sharing data that would otherwise pile up in the drawer because of disappointing results or the lack of time for preparing a regular article. The leading scientometrics platforms Clarivate Analytics, Google Scholar and Scopus should index data journals equally with regular journals to motivate researchers publishing their data. There should be a possibility of article withdrawal by the publisher, if the data availability statements are incorrect or the data have been removed post-acceptance30. Much of the workload should stay on the editors who are paid by the supporting association, institution or publisher in most cases. The editors should grant the referees access to these data during the reviewing process48, requesting them a second opinion about data availability and reasons for declining to do so. Similar stringent data sharing policies are increasingly implemented by various journals26,30,47.In conclusion, data availability in top scientific journals differs strongly by discipline, but it is improving in most research fields. As our study exemplifies, the ‘data availability upon request’ model is insufficient to ensure access to datasets and other critical materials. Considering the overall data availability patterns, authors’ concerns and reasons for declining data sharing, we advocate that (a) data releasing costs ought to be covered by funders; (b) shared data and the associated bibliometric records should be included in the evaluation of job and grant applications; and (c) data sharing enforcement should be led by both funding agencies and academic publishers. More

  • in

    Madrepora oculata forms large frameworks in hypoxic waters off Angola (SE Atlantic)

    1.Roberts, J. M., Wheeler, A. J., Freiwald, A. & Cairns, S. D. Cold-Water Corals. The Biology and Geology of Deep-Sea Coral Habitats. (Cambridge University Press, 2009).2.Davies, A. J. & Guinotte, J. M. Global habitat suitability for framework-forming cold-water corals. Plos One 6, e18483 (2011).3.Morato, T. et al. Climate-induced changes in the suitable habitat of cold-water corals and commercially important deep-sea fishes in the North Atlantic. Glob. Chang. Biol. 26, 2181–2202. https://doi.org/10.1111/gcb.14996 (2020).ADS 
    Article 
    PubMed Central 

    Google Scholar 
    4.Arnaud-Haond, S. et al. Two “pillars” of cold-water coral reefs along Atlantic European margins: Prevalent association of Madrepora oculata with Lophelia pertusa, from reef to colony scale. Deep-Sea Res. Pt. II(145), 110–119 (2017).Article 

    Google Scholar 
    5.Buhl-Mortensen, L., Olafsdottir, S. H., Buhl-Mortensen, P., Burgos, J. M. & Ragnarsson, S. A. Distribution of nine cold-water coral species (Scleractinia and Gorgonacea) in the cold temperate North Atlantic: Effects of bathymetry and hydrography. Hydrobiologia 759, 39–61. https://doi.org/10.1007/s10750-014-2116-x (2015).CAS 
    Article 

    Google Scholar 
    6.Gori, A. et al. Bathymetrical distribution and size structure of cold-water coral populations in the Cap de Creus and Lacaze-Duthiers canyons (northwestern Mediterranean). Biogeosciences 10, 2049–2060. https://doi.org/10.5194/bg-10-2049-2013 (2013).ADS 
    Article 

    Google Scholar 
    7.Orejas, C. et al. Cold-water corals in the Cap de Creus canyon (north-western Mediterranean): Spatial distribution, density and anthropogenic impact. Mar. Ecol. Prog. Ser. 397, 37–51 (2009).ADS 
    Article 

    Google Scholar 
    8.Buhl-Mortensen, P. Coral reefs in the Southern Barents Sea: Habitat description and the effects of bottom fishing. Mar. Biol. Res. 13, 1027–1040. https://doi.org/10.1080/17451000.2017.1331040 (2017).Article 

    Google Scholar 
    9.Cairns, S. Antarctic and subantarctic Scleractinia. Antarctic Res. Ser. 34. https://doi.org/10.1029/AR034p0001 (1983).10.Cairns, S. D. & Zibrowius, H. Cnidaria Anthozoa: Azooxanthellate Scleractinia from the Philippine and Indonesian regions. Mém. Mus. Natl. Hist. Nat. 172, 27–243 (1997).
    Google Scholar 
    11.Tracey, D., Rowden, A., Mackay, K. & Compton, T. Habitat-forming cold-water corals show affinity for seamounts in the New Zealand region. Mar. Ecol. Prog. Ser. 430, 1–22. https://doi.org/10.3354/meps09164 (2011).ADS 
    Article 

    Google Scholar 
    12.Auscavitch, S. R. et al. Oceanographic drivers of deep-sea coral species distribution and community assembly on seamounts, islands, atolls, and reefs within the Phoenix Islands protected area. Front. Mar. Sci. 7. https://doi.org/10.3389/fmars.2020.00042 (2020).13.Angeletti, L., Castellan, G., Montagna, P., Remia, A. & Taviani, M. “The Corsica channel cold-water coral province” (Mediterranean Sea). Front. Mar. Sci. 7. https://doi.org/10.3389/fmars.2020.00661 (2020).14.Chimienti, G., Bo, M., Taviani, M. & Mastrototaro, F. in Mediterranean Cold-Water Corals: Past, Present and Future, Springer Series: Coral Reefs of the World (eds. Covadonga Orejas Saco del Valle & C. Jiménez) 213–243 (Springer, 2019).15.Corbera, G. et al. Ecological characterisation of a Mediterranean cold-water coral reef: Cabliers Coral Mound Province (Alboran Sea, western Mediterranean). Prog. Oceanogr. 175, 245–262. https://doi.org/10.1016/j.pocean.2019.04.010 (2019).ADS 
    Article 

    Google Scholar 
    16.Freiwald, A. et al. The White Coral Community in the Central Mediterranean Sea revealed by ROV surveys. Oceanography 22, 58–74 (2009).Article 

    Google Scholar 
    17.Fabri, M. C. et al. Megafauna of vulnerable marine ecosystems in French Mediterranean submarine canyons: Spatial distribution and anthropogenic impacts. Deep-Sea Res. Pt. II(104), 184–207. https://doi.org/10.1016/j.dsr2.2013.06.016 (2014).Article 

    Google Scholar 
    18.Brooke, S. & Ross, S. W. First observations of the cold-water coral Lophelia pertusa in mid-Atlantic canyons of the USA. Deep-Sea Res. Pt. II(104), 245–251 (2014).Article 

    Google Scholar 
    19.Cordes, E. E. et al. Coral communities of the deep Gulf of Mexico. Deep-Sea Res. Pt. II(55), 777–787 (2008).Article 

    Google Scholar 
    20.Frederiksen, R., Jensen, A. & Westerberg, H. The distribution of scleratinian coral Lophelia pertusa around the Faroe Islands and the relation to intertidal mixing. Sarsia 77, 157–171 (1992).Article 

    Google Scholar 
    21.Hebbeln, D. et al. Environmental forcing of the Campeche cold-water coral province, southern Gulf of Mexico. Biogeosciences 11, 1799–1815. https://doi.org/10.5194/bg-11-1799-2014 (2014).ADS 
    Article 

    Google Scholar 
    22.Wienberg, C. et al. Franken Mound: Facies and biocoenoses on a newly-discovered “carbonate mound” on the western Rockall Bank, NE Atlantic. Facies 54, 1–24. https://doi.org/10.1007/s10347-007-0118-0 (2008).Article 

    Google Scholar 
    23.Purser, A. et al. Local variation in the distribution of benthic megafauna species associated with cold-water coral reefs on the Norwegian margin. Cont. Shelf Res. 54, 37–51. https://doi.org/10.1016/j.csr.2012.12.013 (2013).ADS 
    Article 

    Google Scholar 
    24.Fanelli, E. et al. Cold-water coral Madrepora oculata in the eastern Ligurian Sea (NW Mediterranean): Historical and recent findings. Aquat. Conserv. 27, 965–975. https://doi.org/10.1002/aqc.2751 (2017).Article 

    Google Scholar 
    25.Naumann, M. S., Orejas, C. & Ferrier-Pagès, C. Species-specific physiological response by the cold-water corals Lophelia pertusa and Madrepora oculata to variations within their natural temperature range. Deep-Sea Res. Pt. II(99), 36–41. https://doi.org/10.1016/j.dsr2.2013.05.025 (2014).CAS 
    Article 

    Google Scholar 
    26.Movilla, J. et al. Resistance of two mediterranean cold-water coral species to low-pH conditions. Water 6, 59–67 (2014).ADS 
    Article 

    Google Scholar 
    27.Dodds, L. A., Roberts, J. M., Taylor, A. C. & Marubini, F. Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxgen change. J. Exp. Mar. Biol. Ecol. 349, 205–214 (2007).CAS 
    Article 

    Google Scholar 
    28.Lunden, J. J., McNicholl, C. G., Sears, C. R., Morrison, C. L. & Cordes, E. E. Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification, warming, and deoxygenation. Front. Mar. Sci. 1. https://doi.org/10.3389/fmars.2014.00078 (2014).29.Ramos, A., Sanz, J. L., Ramil, F., Agudo, L. M. & Presas-Navarro, C. in Deep-Sea Ecosystems Off Mauritania: Research of Marine Biodiversity and Habitats in the Northwest African Margin (eds. Ramos, A., Ramil, F., & Sanz, J.L.) 481–525 (Springer, 2017).30.Wienberg, C. et al. The giant Mauritanian cold-water coral mound province: Oxygen control on coral mound formation. Quat. Sci. Rev. 185, 135–152. https://doi.org/10.1016/j.quascirev.2018.02.012 (2018).ADS 
    Article 

    Google Scholar 
    31.Hanz, U. et al. Environmental factors influencing cold-water coral ecosystems in the oxygen minimum zones on the Angolan and Namibian margins. Biogeosciences 16, 4337–4356 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    32.Hebbeln, D. et al. Cold-water coral reefs thriving under hypoxia. Coral Reefs 39, 853–859. https://doi.org/10.1007/s00338-020-01934-6 (2020).Article 

    Google Scholar 
    33.Montero-Serrano, J.-C. et al. Decadal changes in the mid-depth water mass dynamic of the Northeastern Atlantic margin (Bay of Biscay). Earth Planet. Sci. Lett. 364, 134–144. https://doi.org/10.1016/j.epsl.2013.01.012 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Orejas, C., Gori, A. & Gili, J. M. Growth rates of live Lophelia pertusa and Madrepora oculata cold-water coral species maintained in aquaria. Coral Reefs 27, 255 (2008).ADS 
    Article 

    Google Scholar 
    35.Sabatier, P. et al. 210Pb-226Ra chronology reveals rapid growth rate of Madrepora oculata and Lophelia pertusa on world’s largest cold-water coral reef. Biogeosciences 9, 1253–1265. https://doi.org/10.5194/bg-9-1253-2012 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Sweetman, A. et al. Major impacts of climate change on deep-sea benthic ecosystems. Elementa-Sci. Anthrop. 5, 4. https://doi.org/10.1525/elementa.203 (2017).Article 

    Google Scholar 
    37.Lexerød, N. L. Recruitment models for different tree species in Norway. For. Ecol. Manag. 206, 91–108. https://doi.org/10.1016/j.foreco.2004.11.001 (2005).Article 

    Google Scholar 
    38.Georgian, S. et al. Biogeographic variability in the physiological response of the cold-water coral Lophelia pertusa to ocean acidification. Mar. Ecol. 37. https://doi.org/10.1111/maec.12373 (2016).39.Tamborrino, L. et al. Mid-Holocene extinction of cold-water corals on the Namibian shelf steered by the Benguela oxygen minimum zone. Geology 47, 1185–1188. https://doi.org/10.1130/g46672.1 (2019).ADS 
    Article 

    Google Scholar 
    40.Büscher, J., Form, A. & Riebesell, U. Interactive effects of ocean acidification and warming on growth, fitness and survival of the cold-water coral Lophelia pertusa under different food availabilities. Front. Mar. Sci. 4. https://doi.org/10.3389/fmars.2017.00101 (2017).41.Connolly, S., Lopez-Yglesias, M. & Anthony, K. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs 31. https://doi.org/10.1007/s00338-012-0925-9 (2012).42.Middelburg, J. J. et al. Discovery of symbiotic nitrogen fixation and chemoautotrophy in cold-water corals. Sci. Rep. 5, 17962. https://doi.org/10.1038/srep17962 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Wienberg, C. & Titschack, J. in Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots (eds. Rossi, S., Bramanti, L., Gori, A., & del Valle, C.O.S.) 699–732 (Springer, 2017).44.Behrenfeld, M. J. & Falkowski, P. G. Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol. Oceanogr. 42, 1–20 (1997).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Levitus, S. & Mishonov, A. World Ocean Atlas 2013 (Vers. 2). NOAA Atlas NESDIS 73. National Oceanographic Data Center, Ocean Climate Laboratory United States, National Environmental Satellite Data Information Service (2013).46.Mienis, F. et al. Hydrodynamic controls on cold-water coral growth and carbonate-mound development at the SW and SE Rockall Trough Margin, NE Atlantic Ocean. Deep-Sea Res. Pt. I(54), 1655–1674 (2007).Article 

    Google Scholar 
    47.Sanfilippo, R. et al. Serpula aggregates and their role in deep-sea coral communities in the southern Adriatic Sea. Facies 59. https://doi.org/10.1007/s10347-012-0356-7 (2013).48.Hoey, J. A. & Pinsky, M. L. Genomic signatures of environmental selection despite near-panmixia in summer flounder. Evolut. Appl. 11, 1732–1747. https://doi.org/10.1111/eva.12676 (2018).CAS 
    Article 

    Google Scholar 
    49.Boavida, J., Becheler, R., Addamo, A. M., Sylvestre, F. & Arnaud-Haond, S. in Mediterranean Cold-Water Corals: Past, Present and Future, Springer Series: Coral Reefs of the World (eds. Covadonga Orejas Saco del Valle & C. Jiménez) (Springer, 2019).50.Sanford, E. & Kelly, M. W. Local adaptation in marine invertebrates. Ann. Rev. Mar. Sci. 3, 509–535. https://doi.org/10.1146/annurev-marine-120709-142756 (2011).Article 
    PubMed 

    Google Scholar 
    51.Frank, N. et al. Northeastern Atlantic cold-water coral reefs and climate. Geology 39, 743–746. https://doi.org/10.1130/g31825.1 (2011).ADS 
    Article 

    Google Scholar 
    52.Hebbeln, D. et al. ANNA cold-water coral ecosystems off Angola and Namibia. Cruise No. M122, December 30, 2015–January 31, 2016, Walvis Bay (Namibia) – Walvis Bay (Namibia). METEOR-Berichte, M122. DFG-Senatskommission Ozeanogr. 74. https://doi.org/10.2312/cr_m122 (2017).53.Vad, J., Orejas, C., Moreno-Navas, J., Findlay, H. S. & Roberts, J. M. Assessing the living and dead proportions of cold-water coral colonies: Implications for deep-water marine protected area monitoring in a changing ocean. PeerJ 5, e3705. https://doi.org/10.7717/peerj.3705 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Computational sustainability meets materials science

    Computational sustainability research has been supported by an Expedition in Computing from the US National Science Foundation (NSF; CCF-1522054). eBird has been supported by the Leon Levy Foundation, the Wolf Creek Foundation, and NSF (DBI-1939187). Materials science research has also been supported by the AFOSR Multidisciplinary University Research Initiative (MURI) Program FA9550-18-1-0136, US DOE Award No.DE-SC0020383, and an award from the Toyota Research Institute. More