More stories

  • in

    Sexual competition and kin recognition co-shape the traits of neighboring dioecious Diospyros morrisiana seedlings

    1.Karban, R. Plant behaviour and communication. Ecol. Lett. 11, 727–739 (2008).PubMed 
    Article 

    Google Scholar 
    2.Chen, B. J. W., During, H. J. & Anten, N. P. R. Detect the neighbor: Identity recognition at the root level in plants. Plant Sci. 195, 157–167 (2012).PubMed 
    Article 
    CAS 

    Google Scholar 
    3.Inderjit, Seastedt, T. R. et al. Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol. Invasions 10, 875–890 (2008).Article 

    Google Scholar 
    4.Yang, X., Li, L., Xu, Y. & Kong, C. Kin recognition in rice (Oryza sativa) lines. New Phytol 220, 567–578 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    5.Kasperbauer, M. J. & Hunt, P. G. Shoot/root assimilate allocation and nodulation of vigna unguiculata seedlings as influenced by shoot light environment. Plant Soil 161, 97–101 (1994).Article 

    Google Scholar 
    6.Yu, P., Hochholdinger, F. & Li, C. Plasticity of lateral root branching in maize. Front. Plant Sci. 10, 363 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Fang, S. et al. Genotypic recognition and spatial responses by rice roots. Proc. Natl Acad. Sci. USA 110, 2670–2675 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Biedrzycki, M. L., Jilany, T. A., Dudley, S. A. & Bais, H. P. Root exudates mediate kin recognition in plants. Commun. Integr. Biol. 3, 28–35 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Wilczek, A. M. et al. Effects of genetic perturbation on seasonal life history plasticity. Science 323, 930–934 (2009).PubMed 
    Article 
    CAS 

    Google Scholar 
    10.Bhatt, M. V., Khandelwal, A. & Dudley, S. A. Kin recognition, not competitive interactions, predicts root allocation in young Cakile edentula seedling pairs. N. Phytol. 189, 1135–1142 (2011).Article 

    Google Scholar 
    11.Mercer, C. A. & Eppley, S. M. Kin and sex recognition in a dioecious grass. Plant Ecol. 215, 845–852 (2014).Article 

    Google Scholar 
    12.Dong, T., Li, J., Liao, Y., Chen, B. J. W. & Xu, X. Root-mediated sex recognition in a dioecious tree. Sci. Rep. 7, 1–7 (2017).Article 
    CAS 

    Google Scholar 
    13.Renner. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101, 1588–1596 (2014).PubMed 
    Article 

    Google Scholar 
    14.Lovett Doust, J., O’Brien, G. & Lovett Doust, L. Effect of density on secondary sex characteristics and sex ratio in Silene alba (Caryophyllaceae). Am. J. Bot. 74, 40–46 (1987).Article 

    Google Scholar 
    15.Eppley, S. M. Females make tough neighbors: sex-specific competitive effects in seedlings of a dioecious grass. Oecologia 146, 549–554 (2006).PubMed 
    Article 

    Google Scholar 
    16.Graff, P., Rositano, F. & Aguiar, M. R. Changes in sex ratios of a dioecious grass with grazing intensity: the interplay between gender traits, neighbour interactions and spatial patterns. J. Ecol. 101, 1146–1157 (2013).Article 

    Google Scholar 
    17.Dudley, S. A. & File, A. L. Kin recognition in an annual plant. Biol. Lett. 3, 435–438 (2007).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Semchenko, M., Saar, S. & Lepik, A. Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. N. Phytol. 204, 631–637 (2014).Article 

    Google Scholar 
    19.Li, J., Xu, X. L. & Liu, Y. R. Kin recognition in plants with distinct lifestyles: implications of biomass and nutrient niches. Plant Growth Regul. 84, 333–339 (2018).Article 
    CAS 

    Google Scholar 
    20.Lepik, A., Abakumova, M., Zobel, K. & Semchenko, M. Kin recognition is density-dependent and uncommon among temperate grassland plants. Funct. Ecol. 26, 1214–1220 (2012).Article 

    Google Scholar 
    21.Murphy, G. P. & Dudley, S. A. Kin recognition: Competition and cooperation in Impatiens (Balsaminaceae). Am. J. Bot. 96, 1990–1996 (2009).PubMed 
    Article 

    Google Scholar 
    22.Rogers, S. R. & Eppley, S. M. Testing the interaction between inter-sexual competition and phosphorus availability in a dioecious gras. Botany 710, 704–710 (2012).Article 
    CAS 

    Google Scholar 
    23.Bierzychudek, P. & Eckhart, V. Spatial segregation of the sexes of dioecious plants. Am. Nat. 132, 34–43 (1988).Article 

    Google Scholar 
    24.Mercer, C. A. Spatial segregation of the sexes in a salt marsh grass Distichlis spicata (Poaceae). Master Thesis, Portland State University, Portland, Oregon, USA. https://doi.org/10.15760/etd.173 (Portland State University, 2010).25.Hamilton, W. D. The genetical evolution of social behavior, I & II. J. Theor. Biol. 7, 1–52 (1964).PubMed 
    Article 
    CAS 

    Google Scholar 
    26.Haichar, Z. & Bernard, C. Root exudates mediated interactions belowground. Soil Biol. Biochem. 77, 69–80 (2014).Article 
    CAS 

    Google Scholar 
    27.Biedrzycki, M. L., Venkatachalam, L. & Bais, H. P. Transcriptome analysis of Arabidopsis thaliana plants in response to kin and stranger recognition. Plant Signal. Behav. 6, 1515–1524 (2011).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    28.Zhu, S. et al. Effects of root exudates on the growth and development of male and female Morus alba seedlings. Plant Physiol. J. 52, 134–140 (2016).
    Google Scholar 
    29.Mercer, C. A. & Eppley, S. M. Inter-sexual competition in a dioecious grass. Oecologia 164, 657–664 (2010).PubMed 
    Article 

    Google Scholar 
    30.Herrera, C. M. Plant size, spacing patterns, and host-plant selection in Osyris Quadripartita, a hemiparasitic dioecious shrub. J. Ecol. 76, 995–1006 (1988).Article 

    Google Scholar 
    31.Yangxia, Z., Fengyun, L. E. I., Shuang, Q. I. U. & Shanmei, Z. Effects of fatty acid ester compounds on growth and physiological characteristics of water melon seedlings. J. Hunan Agric. Univ. Sci. 46, 297–302 (2020).
    Google Scholar 
    32.Huimin, L. I. et al. The special bacterial metabolites and allelopathic potentials in Casuarina equisetifolia woodland of different stand ages. Chin. J. Appl. Environ. Biol. 22, 808–814 (2016).
    Google Scholar 
    33.Zhang, Jhong, Sun, Hlong, Chen, Syang, Zeng, L. I. & Wang, Ttao Anti-fungal activity, mechanism studies on α-Phellandrene and Nonanal against Penicillium cyclopium. Bot. Stud. 58, 1–9 (2017).Article 
    CAS 

    Google Scholar 
    34.Zhou, T. et al. Effects of essential oil decanal on growth and transcriptome of the postharvest fungal pathogen Penicillium expansum. Postharvest Biol. Technol. 145, 203–212 (2018).Article 
    CAS 

    Google Scholar 
    35.Varga, S. Effects of arbuscular mycorrhizas on reproductive traits in sexually dimorphic plants. J. Agric. Res. 8, 11–24 (2010).
    Google Scholar 
    36.Varga, S. Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. N. Phytol. 199, 812–821 (2013).Article 

    Google Scholar 
    37.Varga, S., Vega-Frutis, R. & Kytöviita, M.-M. Competitive interactions are mediated in a sex-specific manner by arbuscular mycorrhiza in Antennaria dioica. Plant Biol. 19, 217–226 (2017).PubMed 
    Article 
    CAS 

    Google Scholar 
    38.Varga, S. Effects of arbuscular mycorrhizal fungi and maternal plant sex on seed germination and early plant establishment. Am. J. Bot. 102, 358–366 (2015).PubMed 
    Article 

    Google Scholar 
    39.Bawa, K. S. Evolution of dioecy in flowering plants. Annu. Rev. Ecol. Syst. 11, 15–39 (1980).Article 

    Google Scholar 
    40.Zheng, D.-S., Liu, X. & Li, Y. Cultivated plants originated in China. J. Plant Genet. Resour. 13, 1–10 (2012).
    Google Scholar 
    41.Fang, S., Yan, X. & Liao, H. 3D reconstruction and dynamic modeling of root architecture in situ and its application to crop phosphorus research. Plant J. 60, 1096–1108 (2009).PubMed 
    Article 
    CAS 

    Google Scholar 
    42.Akagi, T. et al. Development of molecular markers associated with sexuality in Diospyros lotus L. and their application in D. kaki Thunb. J. Jpn. Soc. Hortic. Sci. 83, 214–221 (2014).Article 
    CAS 

    Google Scholar 
    43.Akagi, T., Henry, I. M., Tao, R. & Comai, L. A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 346, 646–650 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    44.Badri, D. V. et al. Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J. Biol. Chem. 288, 4502–4512 (2013).45.Fiehn, O. et al. Quality control for plant metabolomics: reporting MSI-compliant studies. Plant J. 53, 691–704 (2008).Article 
    CAS 

    Google Scholar 
    46.Lenth, R. V. Least-squares means: the {R} package {lsmeans}. J. Stat. Softw. 69, 1–33 (2016).Article 

    Google Scholar 
    47.Paine, C. E. T. et al. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods Ecol. Evol. 3, 245–256 (2012).Article 

    Google Scholar 
    48.R Core Team. R: A Language and Environment for Statistical Computing (2017). More

  • in

    Parental selection for growth and early-life low stocking density increase the female-to-male ratio in European sea bass

    1.Baroiller, J. F., Cotta, H. & Saillant, E. Environmental effects on fish sex determination and differentiation. Sex. Develop. 3, 118–135 (2009).CAS 
    Article 

    Google Scholar 
    2.Conover, D. O. & Kynard, B. E. Environmental sex determination: interaction of temperature and genotype in a fish. Science 213, 577–579 (1981).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Ospina-Álvarez, N. & Piferrer, F. Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS ONE 3, e2837 (2008).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    4.Geffroy, B. & Wedekind, C. Effects of global warming on sex ratios in fishes. J. Fish Biol. 97, 596–606 (2020).PubMed 
    Article 

    Google Scholar 
    5.Römer, U. & Beisenherz, W. Environmental determination of sex in Apistogrammai (Cichlidae) and two other freshwater fishes (Teleostei). J. Fish Biol. 48, 714–725 (1996).
    Google Scholar 
    6.Geffroy, B. & Bardonnet, A. Sex differentiation and sex determination in eels: consequences for management. Fish Fish 17, 375–398 (2016).Article 

    Google Scholar 
    7.Ribas, L., Valdivieso, A., Díaz, N. & Piferrer, F. Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response. J. Exp. Biol. 220, 1056–1064 (2017).PubMed 
    Article 

    Google Scholar 
    8.Hattori, R. S., Castañeda-Cortés, D. C., Arias Padilla, L. F., Strobl-Mazzulla, P. H. & Fernandino, J. I. Activation of stress response axis as a key process in environment-induced sex plasticity in fish. Cell. Mol. Life Sci. https://doi.org/10.1007/s00018-020-03532-9 (2020).Article 
    PubMed 

    Google Scholar 
    9.Mommsen, T. P., Vijayan, M. M. & Moon, T. W. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fisheries 9, 211–268 (1999).Article 

    Google Scholar 
    10.Prunet, P., Sturm, A. & Milla, S. Multiple corticosteroid receptors in fish: From old ideas to new concepts. Gen. Comp. Endocrinol. 147, 17–23 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Manna, P. R., Dyson, M. T. & Stocco, D. M. Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol. Hum. Reprod. 15, 321–333 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Nematollahi, M. A., van Pelt-Heerschap, H. & Komen, J. Transcript levels of five enzymes involved in cortisol synthesis and regulation during the stress response in common carp: relationship with cortisol. Gen. Comp. Endocrinol. 164, 85–90 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Wu, X. et al. Integration of ATAC-seq and RNA-seq unravels chromatin accessibility during sex reversal in orange-spotted grouper (Epinephelus coioides). Int. J. Mol. Sci. 21, 2800 (2020).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    14.Blasco, M. et al. Molecular characterization of cyp11a1 and cyp11b1 and their gene expression profile in pejerrey (Odontesthes bonariensis) during early gonadal development. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 156, 110–118 (2010).Article 
    CAS 

    Google Scholar 
    15.Todd, E. V. et al. Stress, novel sex genes, and epigenetic reprogramming orchestrate socially controlled sex change. Sci. Adv. 5, eaaw7006 (2019).16.Fernandino, J. I., Hattori, R. S., Moreno Acosta, O. D., Strüssmann, C. A. & Somoza, G. M. Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen. Comparat. Endocrinol. 192, 36–44 (2013).CAS 
    Article 

    Google Scholar 
    17.Geffroy, B. & Douhard, M. The adaptive sex in stressful environments. Trends Ecol. Evol. 34, 628–640 (2019).PubMed 
    Article 

    Google Scholar 
    18.Chiba, H., Iwata, M., Yakoh, K., Satoh, R.-I. & Yamada, H. Possible influence of social stress on sex differentiation in Japanese eel. Fish. Sci. 68, 413–414 (2002).Article 

    Google Scholar 
    19.Hoseini, S. M., Pérez-Jiménez, A., Costas, B., Azeredo, R. & Gesto, M. Physiological roles of tryptophan in teleosts: current knowledge and perspectives for future studies. Rev. Aquac. 11, 3–24 (2019).Article 

    Google Scholar 
    20.Vandeputte, M., Gagnaire, P.-A. & Allal, F. The European sea bass: a key marine fish model in the wild and in aquaculture. Anim. Genet. https://doi.org/10.1111/age.12779 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Vandeputte, M., Dupont-Nivet, M., Chavanne, H. & Chatain, B. B. A polygenic hypothesis for sex determination in the European Sea Bass Dicentrarchus labrax. Genetics 176, 1049–1057 (2007).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Piferrer, F., Blazquez, M., Navarro, L. & Gonzalez, A. Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen. Comparat. Endocrinol. 142, 102–110 (2005).CAS 
    Article 

    Google Scholar 
    23.Vandeputte, M. & Piferrer, F. Genetic and environmental components of sex determination in the European sea bass (Dicentrarchus labrax). In Sex Control in Aquaculture Vol. I (eds. Wang, H. P., Piferrer, F. & Chen, S. L.) 307–325 (John Wiley and Sons, 2019).24.Bláquez, M., Zanuy, S., Carillo, M. & Piferrer, F. Effects of rearing temperature on sex differentiation in the European sea bass (Dicentrarchus labrax L.). J. Exp. Zool. 281, 207–216 (1998).Article 

    Google Scholar 
    25.Saillant, E. et al. Temperature effects and genotype-temperature interactions on sex determination in the European sea bass (Dicentrarchus labrax L.). J. Exp. Zool. 292, 494–505 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    26.Vandeputte, M. et al. Low temperature has opposite effects on sex determination in a marine fish at the larval/postlarval and juvenile stages. Ecol. Evol. 10, 13825 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Saillant, E. et al. Effects of rearing density, size grading and parental factors on sex ratios of the sea bass (Dicentrarchus labrax L) in intensive aquaculture. Aquaculture 221, 183–206 (2003).Article 

    Google Scholar 
    28.Faggion, S. et al. Sex dimorphism in European sea bass (Dicentrarchus labrax L.): new insights into sex-related growth patterns during very early life stages. PLoS ONE 16, e0239791 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Ferrari, S. et al. Early individual electronic identification of sea bass using RFID microtags: a first example of early phenotyping of sex-related growth. Aquaculture 426–427, 165–171 (2014).Article 

    Google Scholar 
    30.Besson, M. et al. Influence of water temperature on the economic value of growth rate in fish farming: the case of sea bass (Dicentrarchus labrax) cage farming in the Mediterranean. Aquaculture 462, 47–55 (2016).Article 

    Google Scholar 
    31.Blázquez, M., González, A., Papadaki, M., Mylonas, C. & Piferrer, F. Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax). Gen. Comp. Endocrinol. 158, 95–101 (2008).PubMed 
    Article 
    CAS 

    Google Scholar 
    32.Ribas, L. et al. Characterization of the European Sea Bass (Dicentrarchus labrax) gonadal transcriptome during sexual development. Mar Biotechnol 21, 359–373 (2019).CAS 
    Article 

    Google Scholar 
    33.Pavlidis, M. et al. Onset of the primary stress in European sea bass Dicentrarhus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development. Aquaculture 315, 125–130 (2011).CAS 
    Article 

    Google Scholar 
    34.Tsalafouta, A. et al. Ontogenesis of the HPI axis and molecular regulation of the cortisol stress response during early development in Dicentrarchus labrax. Sci. Rep. 4, (2014).35.Alfonso, S., Gesto, M. & Sadoul, B. Temperature increase and its effects on fish stress physiology in the context of global warming. J. Fish Biol. https://doi.org/10.1111/jfb.14599 (2020).Article 
    PubMed 

    Google Scholar 
    36.Goikoetxea, A. et al. Genetic pathways underpinning hormonal stress responses in fish exposed to short- and long-term warm ocean temperatures. Ecol. Indic. 120, 106937 (2021).Article 

    Google Scholar 
    37.Bertotto, D. et al. Alternative matrices for cortisol measurement in fish. Aquac. Res. 41, 1261–1267 (2010).CAS 

    Google Scholar 
    38.Sadoul, B., Leguen, I., Colson, V., Friggens, N. C. & Prunet, P. A multivariate analysis using physiology and behavior to characterize robustness in two isogenic lines of rainbow trout exposed to a confinement stress. Physiol. Behav. 140, 139–147 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Simontacchi, C. et al. Alternative stress indicators in sea bass Dicentrarchus labrax L. J. Fish Biol. 72, 747–752 (2008).Article 

    Google Scholar 
    40.Zuberi, A., Brown, C. & Ali, S. Effect of confinement on water-borne and whole body cortisol in wild and captive-reared rainbowfish (Melanoteania duboulayi). Int. J. Agric. Biol. 16, 183–188 (2014).41.Cortés, D. C. C., Padilla, L. F. A., Langlois, V. S., Somoza, G. M. & Fernandino, J. I. The central nervous system acts as a transducer of stress-induced masculinization through corticotropin-releasing hormone B. Development 146, (2019).42.Faught, E. & Vijayan, M. M. The mineralocorticoid receptor is essential for stress axis regulation in zebrafish larvae. Sci. Rep. 8, 18081 (2018).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Kiilerich, P., Geffroy, B., Valotaire, C. & Prunet, P. Endogenous regulation of 11-deoxycorticosterone (DOC) and corticosteroid receptors (CRs) during rainbow trout early development and the effects of corticosteroids on hatching. Gen. Comp. Endocrinol. https://doi.org/10.1016/j.ygcen.2018.05.031 (2018).Article 
    PubMed 

    Google Scholar 
    44.Rosengren, M., Thörnqvist, P.-O., Winberg, S. & Sundell, K. The brain-gut axis of fish: Rainbow trout with low and high cortisol response show innate differences in intestinal integrity and brain gene expression. Gen. Comp. Endocrinol. 257, 235–245 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Kiilerich, P. et al. Regulation of the corticosteroid signalling system in rainbow trout HPI axis during confinement stress. Gen. Comp. Endocrinol. 258, 184–193 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    46.Stolte, E. H. et al. Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. J. Endocrinol. 198, 403–417 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Madaro, A. et al. Stress in Atlantic salmon: response to unpredictable chronic stress. J. Exp. Biol. 218, 2538–2550 (2015).PubMed 

    Google Scholar 
    48.Aerts, J. et al. Scales tell a story on the stress history of fish. PLOS ONE 10, e0123411 (2015).49.Moltesen, M. et al. Effects of acute and chronic stress on telencephalic neurochemistry and gene expression in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 219, 3907–3914 (2016).PubMed 

    Google Scholar 
    50.Smith, B. R. Sea lampreys in the Great Lakes of North America. 207–247 (1971).51.García-Cruz, E. L. et al. Crowding stress during the period of sex determination causes masculinization in pejerrey Odontesthes bonariensis, a fish with temperature-dependent sex determination. Comparat. Biochem. Physiol. A: Mol. Integrat. Physiol. 245, 110701 (2020).Article 
    CAS 

    Google Scholar 
    52.Vandeputte, M. & Piferrer, F. Genetic and Environmental Components of Sex Determination in the European Sea Bass. In Sex Control in Aquaculture 305–325 (John Wiley & Sons, Ltd, 2018). https://doi.org/10.1002/9781119127291.ch14.53.Díaz, N., Ribas, L. & Piferrer, F. The relationship between growth and sex differentiation in the European sea bass (Dicentrarchus labrax). Aquaculture 408–409, 191–202 (2013).Article 

    Google Scholar 
    54.Papadaki, M. et al. Growth, sex differentiation and gonad and plasma levels of sex steroids in male- and female-dominant populations of Dicentrarchus labrax obtained through repeated size grading. J. Fish Biol. 66, 938–956 (2005).CAS 
    Article 

    Google Scholar 
    55.Sadoul, B. & Vijayan, M. M. 5 – Stress and Growth. In Fish Physiology Vol. 35 (eds. Schreck, C. B., Tort, L., Farrell, A. P. & Brauner, C. J.) 167–205 (Academic Press, 2016).56.Sakae, Y. et al. Starvation causes female-to-male sex reversal through lipid metabolism in the teleost fish, medaka (Olyzias latipes). Biology Open 9, (2020).57.Höglund, E., Øverli, Ø. & Winberg, S. Tryptophan metabolic pathways and brain serotonergic activity: a comparative review. Front. Endocrinol. 10, (2019).58.Amri, A. et al. Effect of melatonin and folic acid supplementation on the growth performance, antioxidant status, and liver histology of the farmed gilthead sea bream (Sparus aurata L.) under standard rearing conditions. Fish Physiol. Biochem. 46, 2265–2280 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.de Pedro, N., Pinillos, M. L., Valenciano, A. I., Alonso-Bedate, M. & Delgado, M. J. Inhibitory effect of serotonin on feeding behavior in goldfish: involvement of CRF. Peptides 19, 505–511 (1998).PubMed 
    Article 

    Google Scholar 
    60.Papoutsoglou, S. E., Karakatsouli, N. & Chiras, G. Dietary l-tryptophan and tank colour effects on growth performance of rainbow trout (Oncorhynchus mykiss) juveniles reared in a recirculating water system. Aquacult. Eng. 32, 277–284 (2005).Article 

    Google Scholar 
    61.Lam, D. D., Garfield, A. S., Marston, O. J., Shaw, J. & Heisler, L. K. Brain serotonin system in the coordination of food intake and body weight. Pharmacol. Biochem. Behav. 97, 84–91 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Tsai, C.-L., Wang, L.-H., Chang, C.-F. & Kao, C.-C. Effects of gonadal steroids on brain serotonergic and aromatase activity during the critical period of sexual differentiation in Tilapia, Oreochromis mossambicus. J. Neuroendocrinol. 12, 894–898 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Raghuveer, K. et al. Gender differences in tryptophan hydroxylase-2 mRNA, serotonin, and 5-hydroxytryptophan levels in the brain of catfish, Clarias gariepinus, during sex differentiation. Gen. Comp. Endocrinol. 171, 94–104 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Sudhakumari, C. C. et al. Dimorphic expression of tryptophan hydroxylase in the brain of XX and XY Nile tilapia during early development. Gen. Comp. Endocrinol. 166, 320–329 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Senthilkumaran, B. et al. “Brain sex differentiation” in teleosts: emerging concepts with potential biomarkers. Gen. Comp. Endocrinol. 220, 33–40 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Carpenter, R. E. et al. Corticotropin releasing factor induces anxiogenic locomotion in trout and alters serotonergic and dopaminergic activity. Horm. Behav. 52, 600–611 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    67.Clements, S. haun, Moore, F. L. & Schreck, C. B. Evidence that acute serotonergic activation potentiates the locomotor-stimulating effects of corticotropin-releasing hormone in juvenile chinook salmon (Oncorhynchus tshawytscha). Horm. Behav. 43, 214–221 (2003).68.Grima, L. et al. In search for indirect criteria to improve feed utilization efficiency in sea bass (Dicentrarchus labrax). Aquaculture 302, 169–174 (2010).Article 

    Google Scholar 
    69.Geffroy, B. et al. Nature-based tourism elicits a phenotypic shift in the coping abilities of fish. Front. Physiol. 9, (2018).70.Sadoul, B. & Geffroy, B. Measuring cortisol, the major stress hormone in fishes. J. Fish Biol. 94, 540–555 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Sadoul, B. et al. Enhanced brain expression of genes related to cell proliferation and neural differentiation is associated with cortisol receptor expression in fishes. Gen. Comp. Endocrinol. 267, 76–81 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Alfonso, S. et al. Coping styles in European sea bass: the link between boldness, stress response and neurogenesis. Physiol. Behav. 207, 76–85 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Samaras, A. & Pavlidis, M. Regulation of divergent cortisol responsiveness in European sea bass, Dicentrarchus labrax L. PLoS ONE 13, e0202195 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    74.Tine, M. et al. European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat. Commun. 5, 5770 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    75.Gesto, M., Skov, P. V. & Jokumsen, A. Emergence time and skin melanin spot patterns do not correlate with growth performance, social competitive ability or stress response in farmed rainbow trout. Front. Neurosci. 11, (2017).76.Menu, B., Peruzzi, S., Vergnet, A., Vidal, M.-O.O. & Chatain, B. A shortcut method for sexing juvenile European sea bass, Dicentrarchus labrax L. Aquacult. Res. 36, 41–44 (2005).Article 

    Google Scholar 
    77.Griot, R. et al. Genome-wide association studies for resistance to viral nervous necrosis in three populations of European sea bass (Dicentrarchus labrax) using a novel 57k SNP array DlabChip. Aquaculture 530, 735930 (2021).78.Griot, R. et al. APIS: An auto-adaptive parentage inference software that tolerates missing parents. Mol. Ecol. Resour. 20, 579–590 (2020).PubMed 
    Article 

    Google Scholar  More

  • in

    Contrasting alien effects on native diversity along biotic and abiotic gradients in an arid protected area

    1.Vilà, M. et al. Ecological impacts of invasive alien plants: A meta-analysis of their effects on species, communities and ecosystems: Ecological impacts of invasive alien plants. Ecol. Lett. 14, 702–708 (2011).PubMed 
    Article 

    Google Scholar 
    2.Pyšek, P. et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species’ traits and environment. Glob. Change Biol. 18, 1725–1737 (2012).ADS 
    Article 

    Google Scholar 
    3.Pyšek, P. et al. Scientists’ warning on invasive alien species. Biol. Rev. 95, 1511–1534 (2020).PubMed 
    Article 

    Google Scholar 
    4.Gordon, D. R. Effects of invasive, non-indigenous plant species on ecosystem processes: Lessons from Florida. Ecol. Appl. 8, 975–989 (1998).Article 

    Google Scholar 
    5.Vieites-Blanco, C. & González-Prieto, S. J. Effects of Carpobrotus edulis invasion on soil gross N fluxes in rocky coastal habitats. Sci. Total Environ. 619–620, 966–976 (2018).ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 
    6.Loiola, P. P. et al. Invaders among locals: Alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J. Ecol. 106, 2230–2241 (2018).Article 

    Google Scholar 
    7.de la Riva, E. G., Godoy, O., Castro-Díez, P., Gutiérrez-Cánovas, C. & Vilà, M. Functional and phylogenetic consequences of plant invasion for coastal native communities. J. Veg. Sci. 30, 510–520 (2019).Article 

    Google Scholar 
    8.Ordonez, A. Functional and phylogenetic similarity of alien plants to co-occurring natives. Ecology 95, 1191–1202 (2014).PubMed 
    Article 

    Google Scholar 
    9.Bezeng, S. B., Davies, J. T., Yessoufou, K., Maurin, O. & der Bank, M. V. Revisiting Darwin’s naturalization conundrum: Explaining invasion success of non-native trees and shrubs in southern Africa. J. Ecol. 103, 871–879 (2015).Article 

    Google Scholar 
    10.Li, S. et al. The effects of phylogenetic relatedness on invasion success and impact: Deconstructing Darwin’s naturalisation conundrum. Ecol. Lett. 18, 1285–1292 (2015).PubMed 
    Article 

    Google Scholar 
    11.Carboni, M. et al. What it takes to invade grassland ecosystems: Traits, introduction history and filtering processes. Ecol. Lett. 19, 219–229 (2016).PubMed 
    Article 

    Google Scholar 
    12.Cadotte, M. W., Campbell, S. E., Li, S., Sodhi, D. S. & Mandrak, N. E. Preadaptation and naturalization of nonnative species: Darwin’s two fundamental insights into species invasion. Annu. Rev. Plant Biol. 69, 661–684 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Diez, J. M., Sullivan, J. J., Hulme, P. E., Edwards, G. & Duncan, R. P. Darwin’s naturalization conundrum: Dissecting taxonomic patterns of species invasions. Ecol. Lett. 11, 674–681 (2008).PubMed 
    Article 

    Google Scholar 
    14.Ma, C. et al. Different effects of invader–native phylogenetic relatedness on invasion success and impact: A meta-analysis of Darwin’s naturalization hypothesis. Proc. R. Society B: Biological Sciences 283, 20160663 (2016).Article 

    Google Scholar 
    15.Bennett, J. A. Similarities between invaders and native species: Moving past Darwin’s naturalization conundrum. J. Veg. Sci. 30, 1027–1034 (2019).Article 

    Google Scholar 
    16.Funk, J. L., Standish, R. J., Stock, W. D. & Valladares, F. Plant functional traits of dominant native and invasive species in mediterranean-climate ecosystems. Ecology 97, 75–83 (2016).PubMed 
    Article 

    Google Scholar 
    17.Daehler, C. C. Darwin’s naturalization hypothesis revisited. Am. Nat. 158, 324–330 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Duncan, R. P. & Williams, P. A. Ecology: Darwin’s naturalization hypothesis challenged. Nature 417, 608 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Ferreira, R. B., Beard, K. H., Peterson, S. L., Poessel, S. A. & Callahan, C. M. Establishment of introduced reptiles increases with the presence and richness of native congeners. Amphibia-Reptilia 33, 387–392 (2012).Article 

    Google Scholar 
    20.Allen, C. R. et al. Predictors of regional establishment success and spread of introduced non-indigenous vertebrates. Glob. Ecol. Biogeogr. 22, 889–899 (2013).Article 

    Google Scholar 
    21.Maitner, B. S., Rudgers, J. A., Dunham, A. E. & Whitney, K. D. Patterns of bird invasion are consistent with environmental filtering. Ecography 35, 614–623 (2012).Article 

    Google Scholar 
    22.Park, D. S. & Potter, D. Why close relatives make bad neighbours: Phylogenetic conservatism in niche preferences and dispersal disproves Darwin’s naturalization hypothesis in the thistle tribe. Mol. Ecol. 24, 3181–3193 (2015).PubMed 
    Article 

    Google Scholar 
    23.Park, D. S. & Potter, D. A reciprocal test of Darwin’s naturalization hypothesis in two mediterranean-climate regions. Glob. Ecol. Biogeogr. 24, 1049–1058 (2015).Article 

    Google Scholar 
    24.Kembel, S. W. & Hubbell, S. P. The phylogenetic structure of a neotropical forest tree community. Ecology 87, S86–S99 (2006).PubMed 
    Article 

    Google Scholar 
    25.Catford, J. A., Jansson, R. & Nilsson, C. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers. Distrib. 15, 22–40 (2009).Article 

    Google Scholar 
    26.Thuiller, W. et al. Resolving Darwin’s naturalization conundrum: a quest for evidence. Divers. Distrib. 16, 461–475 (2010).Article 

    Google Scholar 
    27.Funk, J. L., Cleland, E. E., Suding, K. N. & Zavaleta, E. S. Restoration through reassembly: Plant traits and invasion resistance. Trends Ecol. Evol. 23, 695–703 (2008).PubMed 
    Article 

    Google Scholar 
    28.Lapiedra, O., Sol, D., Traveset, A. & Vilà, M. Random processes and phylogenetic loss caused by plant invasions. Glob. Ecol. Biogeogr. 24, 774–785 (2015).Article 

    Google Scholar 
    29.Castro-Díez, P., Pauchard, A., Traveset, A. & Vilà, M. Linking the impacts of plant invasion on community functional structure and ecosystem properties. J. Veg. Sci. 27, 1233–1242 (2016).Article 

    Google Scholar 
    30.Hulme, P. E. & Bernard-Verdier, M. Evaluating differences in the shape of native and alien plant trait distributions will bring new insights into invasions of plant communities. J. Veg. Sci. 29, 348–355 (2018).Article 

    Google Scholar 
    31.Mayfield, M. M. & Levine, J. M. Opposing effects of competitive exclusion on the phylogenetic structure of communities: Phylogeny and coexistence. Ecol. Lett. 13, 1085–1093 (2010).PubMed 
    Article 

    Google Scholar 
    32.de Bello, F. et al. Functional species pool framework to test for biotic effects on community assembly. Ecology 93, 2263–2273 (2012).PubMed 
    Article 

    Google Scholar 
    33.Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).Article 

    Google Scholar 
    34.Kunstler, G. et al. Competitive interactions between forest trees are driven by species’ trait hierarchy, not phylogenetic or functional similarity: Implications for forest community assembly. Ecol. Lett. 15, 831–840 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Gallien, L. et al. Contrasting the effects of environment, dispersal and biotic interactions to explain the distribution of invasive plants in alpine communities. Biol. Invasions 17, 1407–1423 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Gallien, L. & Carboni, M. The community ecology of invasive species: Where are we and what’s next?. Ecography 40, 335–352 (2017).Article 

    Google Scholar 
    37.Parker, I. M. et al. Impact: Toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1, 3–19 (1999).Article 

    Google Scholar 
    38.Byers, J. E. et al. Directing research to reduce the impacts of nonindigenous species. Conserv. Biol. 16, 630–640 (2002).Article 

    Google Scholar 
    39.Hejda, M., Pyšek, P. & Jarošík, V. Impact of invasive plants on the species richness, diversity and composition of invaded communities. J. Ecol. 97, 393–403 (2009).Article 

    Google Scholar 
    40.Pyšek, P. & Pyšek, A. Invasion by Heracleum mantegazzianum in different habitats in the Czech Republic. J. Veg. Sci. 6, 711–718 (1995).Article 

    Google Scholar 
    41.Hejda, M. & Pyšek, P. What is the impact of Impatiens glandulifera on species diversity of invaded riparian vegetation?. Biol. Conserv. 132, 143–152 (2006).Article 

    Google Scholar 
    42.Chmura, D. et al. The influence of invasive Fallopia taxa on resident plant species in two river valleys (southern Poland). Acta Soc. Bot. Pol. 84, 23–33 (2015).Article 

    Google Scholar 
    43.MacDougall, A. S., Gilbert, B. & Levine, J. M. Plant invasions and the niche. J. Ecol. 97, 609–615 (2009).Article 

    Google Scholar 
    44.Li, S. et al. Contrasting effects of phylogenetic relatedness on plant invader success in experimental grassland communities. J. Appl. Ecol. 52, 89–99 (2015).CAS 
    Article 

    Google Scholar 
    45.Macarthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).Article 

    Google Scholar 
    46.Abrams, P. The theory of limiting similarity. Annu. Rev. Ecol. Syst. 14, 359–376 (1983).Article 

    Google Scholar 
    47.Davies, T. J. Evolutionary ecology: When relatives cannot live together. Evol. Ecol. 16, R645–R647 (2006).ADS 
    CAS 

    Google Scholar 
    48.Omar Kariem, A. Eco-geographical analysis on mountain plants—Kariem Omar—Livres spécialisés. Africa Vivre. https://www.laboutiqueafricavivre.com/livres-specialises/156599-eco-geographical-analysis-on-mountain-plants-9783847331537.html (2012).49.Omar Karim A. Extinction—Towards Plant Conservation. (Lap Lambert Academic Publ, 2014).50.Klute, A. Water retention: Laboratory methods. In: (ed. Klute, A.) Methods of Soil Analysis, Part 1, Physical and Mineralogical Methods, ASA and SSSA, Madison, 635–662. https://doi.org/10.2136/sssabookser5.1.2ed. (1986)Chapter 

    Google Scholar 
    51.Allen, S. E., Grimshaw, H. M., Parkinson, J. A. & Quarmby, C. Chemical Analysis of Ecological Materials. (Blackwell Scientific Publications, 1974).52.Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Pérez-Harguindeguy, N. et al. New handbook for stand-ardised measurement of plant functional traits worldwide. Aust. J. Bot. 61, 167–234 (2013).Article 

    Google Scholar 
    54.Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Wheeler, D. L. GenBank. Nucleic Acids Res. 33, D34-38 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    55.Kück, P. & Meusemann, K. FASconCAT: Convenient handling of data matrices. Mol. Phylogenet. Evol. 56, 1115–1118 (2010).PubMed 
    Article 
    CAS 

    Google Scholar 
    56.Posada, D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Anisimova, M. & Gascuel, O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst. Biol. 55, 539–552 (2006).PubMed 
    Article 

    Google Scholar 
    58.Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003).PubMed 
    Article 

    Google Scholar 
    59.Sanderson, M. J. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Mol. Biol. Evol. 19, 101–109 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Paradis, E., Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Villéger, S., Mason, N. W. H. & Mouillot, D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89, 2290–2301 (2008).Article 

    Google Scholar 
    62.Veron, S., Davies, T. J., Cadotte, M. W., Clergeau, P. & Pavoine, S. Predicting loss of evolutionary history: Where are we?. Biol. Rev. 92, 271–291 (2017).PubMed 
    Article 

    Google Scholar 
    63.Swenson, N. Functional and Phylogenetic Ecology in R. (Springer, 2014). https://doi.org/10.1007/978-1-4614-9542-0.64.Webb, C. O., Ackerly, D. D., McPeek, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002).Article 

    Google Scholar 
    65.Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    66.Blomberg, S. P., Garland, T. Jr. & Ives, A. R. Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57, 717–745 (2003).PubMed 
    Article 

    Google Scholar 
    67.Laliberté, E. & Legendre, P. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010).Article 

    Google Scholar 
    68.Spasojevic, M. J. & Suding, K. N. Inferring community assembly mechanisms from functional diversity patterns: The importance of multiple assembly processes. J. Ecol. 100, 652–661 (2012).Article 

    Google Scholar 
    69.Carboni, M. et al. Functional traits modulate the response of alien plants along abiotic and biotic gradients. Glob. Ecol. Biogeogr. 27, 1173–1185 (2018).Article 

    Google Scholar 
    70.Kruskal, J. B. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29, 1–27 (1964).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    71.Oksanen, J. et al. Vegan: community ecology package. R Package version 2.4-1. https://cran.r-project.org (2016).72.Vila, M. et al. Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J. Biogeogr. 33, 853–861 (2006).Article 

    Google Scholar 
    73.Dong, L.-J., Yu, H.-W. & He, W.-M. What determines positive, neutral, and negative impacts of Solidago canadensis invasion on native plant species richness? Sci Rep. 5(1), 1–9 (2015).CAS 

    Google Scholar 
    74.Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).PubMed 
    Article 

    Google Scholar 
    75.Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    76.Jucker, T., Carboni, M. & Acosta, A. T. R. Going beyond taxonomic diversity: deconstructing biodiversity patterns reveals the true cost of iceplant invasion. Divers. Distrib. 19, 1566–1577 (2013).Article 

    Google Scholar 
    77.Prinzing, A. et al. Less lineages—More trait variation: Phylogenetically clustered plant communities are functionally more diverse. Ecol. Lett. 11, 809–819 (2008).PubMed 
    Article 

    Google Scholar 
    78.Blonder, B. Do hypervolumes have holes?. Am. Nat. 187, E93–E105 (2016).PubMed 
    Article 

    Google Scholar 
    79.Levine, J. M. & D’Antonio, C. M. Elton revisited: A review of evidence linking diversity and invasibility. Oikos 87, 15–26 (1999).Article 

    Google Scholar 
    80.Fargione, J., Brown, C. S. & Tilman, D. Community assembly and invasion: An experimental test of neutral versus niche processes. PNAS 100, 8916–8920 (2003).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Zavaleta, E. S. & Hulvey, K. B. Realistic variation in species composition affects grassland production, resource use and invasion resistance. Plant Ecol 188, 39–51 (2007).Article 

    Google Scholar 
    82.Case, T. J. Invasion resistance arises in strongly interacting species-rich model competition communities. Proc. Natl. Acad. Sci. 87, 9610–9614 (1990).ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    Article 

    Google Scholar 
    83.Kennedy, T. A. et al. Biodiversity as a barrier to ecological invasion. Nature 417, 636 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Gerhold, P. et al. Phylogenetically poor plant communities receive more alien species, which more easily coexist with natives. Am. Nat. 177, 668–680 (2011).PubMed 
    Article 

    Google Scholar 
    85.de Bello, F. et al. Decoupling phylogenetic and functional diversity to reveal hidden signals in community assembly. Methods Ecol. Evol. 8, 1200–1211 (2017).ADS 
    Article 

    Google Scholar 
    86.Cadotte, M. W., Carboni, M., Si, X. & Tatsumi, S. Do traits and phylogeny support congruent community diversity patterns and assembly inferences?. J. Ecol. 107, 2065–2077 (2019).Article 

    Google Scholar 
    87.Lososová, Z. et al. Alien plants invade more phylogenetically clustered community types and cause even stronger clustering. Glob. Ecol. Biogeogr. 24, 786–794 (2015).Article 

    Google Scholar 
    88.Hulme, P. E. & Bernard-Verdier, M. Comparing traits of native and alien plants: Can we do better?. Funct. Ecol. 32, 117–125 (2018).Article 

    Google Scholar 
    89.Luo, Y.-H. et al. Trait-based community assembly along an elevational gradient in subalpine forests: Quantifying the roles of environmental factors in inter- and intraspecific variability. PLoS One 11, e0155749 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    90.Luo, Y.-H. et al. Forest community assembly is driven by different strata-dependent mechanisms along an elevational gradient. J. Biogeogr. 46, 2174–2187 (2019).Article 

    Google Scholar 
    91.Jakobs, G., Weber, E. & Edwards, P. J. Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Divers. Distrib. 10, 11–19 (2004).Article 

    Google Scholar 
    92.Chmura, D. & Sierka, E. The invasibility of deciduous forest communities after disturbance: A case study of Carex brizoides and Impatiens parviflora invasion. For. Ecol. Manag. 242, 487–495 (2007).Article 

    Google Scholar 
    93.Szymura, M. & Szymura, T. H. The dynamics of growth and flowering of invasive Solidago species. Steciana 19, 143–152 (2015).MATH 
    Article 

    Google Scholar 
    94.Divíšek, J. et al. Similarity of introduced plant species to native ones facilitates naturalization, but differences enhance invasion success. Nat. Commun. 9, 4631 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    95.Czarniecka-Wiera, M., Kącki, Z., Chytrý, M. & Palpurina, S. Diversity loss in grasslands due to the increasing dominance of alien and native competitive herbs. Biodivers. Conserv. https://doi.org/10.1007/s10531-019-01794-9 (2019).Article 

    Google Scholar 
    96.Tilman, D. Species richness of experimental productivity gradients: How important is colonization limitation?. Ecology 74, 2179–2191 (1993).Article 

    Google Scholar 
    97.Burke, M. J. W. & Grime, J. P. An experimental study of plant community invasibility. Ecology 77, 776–790 (1996).Article 

    Google Scholar 
    98.Naeem, S. et al. Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91, 97–108 (2000).Article 

    Google Scholar 
    99.Berger, S., Söhlke, G., Walther, G.-R. & Pott, R. Bioclimatic limits and range shifts of cold-hardy evergreen broad-leaved species at their northern distributional limit in Europe. Phytocoenologia 37, 523–539 (2007).Article 

    Google Scholar 
    100.El-Barougy, R. F. et al. Functional similarity and dissimilarity facilitate alien plant invasiveness along biotic and abiotic gradients in an arid protected area. Biol. Invasions 22, 1997–2016 (2020).Article 

    Google Scholar 
    101.Ordonez, A., Wright, I. J. & Olff, H. Functional differences between native and alien species: A global-scale comparison: Functional differences of native and alien plants. Funct. Ecol. 24, 1353–1361 (2010).Article 

    Google Scholar 
    102.Godoy, O. & Levine, J. M. Phenology effects on invasion success: Insights from coupling field experiments to coexistence theory. Ecology 95, 726–736 (2014).PubMed 
    Article 

    Google Scholar 
    103.Cavender-Bares, J., Ackerly, D. D., Baum, D. A. & Bazzaz, F. A. Phylogenetic overdispersion in Floridian Oak Communities. Am. Nat. 163, 823–843 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    104.Richardson, D. M. & Pyšek, P. Plant invasions: Merging the concepts of species invasiveness and community invasibility. Prog. Phys. Geogr. 30, 409–431 (2006).Article 

    Google Scholar 
    105.Pyšek, P., Prach, K. & Smilauer, P. Relating invasion success to plant traits: An analysis of the Czech alien flora. Plant Invasions Gen. Aspects Spec. Probl. 39–60 (1995).
    106.Pyšek, P. et al. Alien plants in temperate weed communities: Prehistoric and recent invaders occupy different habitats. Ecology 86, 772–785 (2005).Article 

    Google Scholar 
    107.Prinzing, A., Durka, W., Klotz, S. & Brandl, R. Which species become aliens?. Evol. Ecol. Res. 4, 385–405 (2002).
    Google Scholar 
    108.van Kleunen, M., Weber, E. & Fischer, M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol. Lett. 13, 235–245 (2010).PubMed 
    Article 

    Google Scholar 
    109.Jauni, M. & Hyvönen, T. Interactions between alien plant species traits and habitat characteristics in agricultural landscapes in Finland. Biol. Invasions 14, 47–63 (2012).Article 

    Google Scholar 
    110.Nentwig, W., Kühnel, E. & Bacher, S. A generic impact-scoring system applied to alien mammals in Europe. Conserv. Biol. 24, 302–311 (2010).PubMed 
    Article 

    Google Scholar 
    111.Liu, P. et al. Urbanization increases biotic homogenization of zooplankton communities in tropical reservoirs. Ecol. Indic. 110, 105899 (2020).Article 

    Google Scholar  More

  • in

    The effects of water control on the survival and growth of Alternanthera philoxeroides in the vegetative reproduction and seedling stages

    1.Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).CAS 
    Article 

    Google Scholar 
    2.Sakai, A. K. et al. The population biology of invasive species. Annu. Rev. Ecol. Evol. Syst. 32, 305–312 (2001).Article 

    Google Scholar 
    3.Buckingham, G. R. Biological control of alligator weed, Alternanthera philoxeroides, the world’s first aquatic weed success story. Castanea 61, 232–243 (1996).
    Google Scholar 
    4.Bassett, I., Paynter, Q., Hankin, R. & Beggs, J. R. Characterising alligator weed (Alternanthera philoxeroides; Amaranthaceae) invasion at a northern New Zealand lake. New Zeal. J. Ecol. 36, 216–222 (2012).
    Google Scholar 
    5.Chatterjee, A. & Dewanji, A. Effect of varying Alternanthera philoxeroides (alligator weed) cover on the macrophyte species diversity of pond ecosystems: A quadrat-based study. Aquat. Invasions 9, 343–355 (2014).Article 

    Google Scholar 
    6.Xu, C. Y., Zhang, W. J., Fu, C. Z. & Lu, B. R. Genetic diversity of alligator weed in China by RAPD analysis. Biodivers. Conserv. 12, 637–645 (2003).Article 

    Google Scholar 
    7.Wang, B. R., Li, W. G. & Wang, J. B. Genetic diversity of Alternanthera philoxeroides in China. Aquat. Bot. 81, 277–283 (2005).Article 

    Google Scholar 
    8.Geng, Y. P. et al. Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener. Acta. Oecol. 30, 380–385 (2006).ADS 
    Article 

    Google Scholar 
    9.Pan, X. Y., Geng, Y. P., Zhang, W. J., Li, B. & Chen, J. K. The influence of abiotic stress and phenotypic plasticity on the distribution of invasive Alternanthera philoxeroides along a riparian zone. Acta. Oecol. 30, 333–341 (2006).ADS 
    Article 

    Google Scholar 
    10.Peng, X. M. et al. Vegetative propagation capacity of invasive alligator weed through small stolon fragments under different treatments. Sci. Rep. 7, 43826. https://doi.org/10.1038/srep43826 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Dugdale, T., Clements, D., Hunt, T. & Butler, K. Alligator weed produces viable stem fragments in response to herbicide treatment. J. Aquat. Plant Manag. 48, 84–91 (2010).
    Google Scholar 
    12.Chen, Y., Zhou, Y., Yin, T. F., Liu, C. X. & Lou, F. L. The invasive wetland plant Alternanthera philoxeroides shows a higher tolerance to waterlogging than its native congener Alternanthera sessilis. PloS One 8, e81456. https://doi.org/10.1371/journal.pone.0081456 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Tao, Y., Chen, F., Wan, K. Y., Li, X. W. & Li, J. Q. The structural adaptation of aerial parts of invasive Alternanthera philoxeroides to water regime. J. Plant Biol. 52, 403–410 (2009).Article 

    Google Scholar 
    14.Wang, N. et al. Clonal integration supports the expansion from terrestrial to aquatic environments of the amphibious stoloniferous herb Alternanthera philoxeroides. Plant Biol. 11, 483–489 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Fan, S. F. et al. The effects of complete submergence on the morphological and biomass allocation response of the invasive plant Alternanthera philoxeroides. Hydrobiologia 746, 159–169 (2015).CAS 
    Article 

    Google Scholar 
    16.Wang, H. F. et al. Effects of submergence on growth, survival and recovery growth of Alternanthera philoxeroides. J. Wuhan Bot. Res. 26, 147–152 (2008).
    Google Scholar 
    17.Zhang, H. J. et al. Effects of submergence and eutrophication on the morphological traits and biomass allocation of the invasive plant Alternanthera philoxeroides. J. Freshw. Ecol. 31, 341–349 (2016).CAS 
    Article 

    Google Scholar 
    18.Sun, J. F. et al. Addition of Phosphorus and nitrogen support the invasiveness of Alternanthera philoxeroides under water stress. Clean Soil Air Water 48, 2000059. https://doi.org/10.1002/clen.202000059 (2020).CAS 
    Article 

    Google Scholar 
    19.Zhou, J., Li, H. L., Alpert, P., Zhang, M. X. & Yu, F. H. Fragmentation of the invasive, clonal plant Alternanthera philoxeroides decreases its growth but not its competitive effect. Flora 228, 17–23 (2017).Article 

    Google Scholar 
    20.Danckwerts, J. E. & Gordon, A. J. Long-term partitioning, storage and remobilization of 14C assimilated by Trifolium repens (cv. Blanc). Ann. Bot. 64, 533–544 (1989).Article 

    Google Scholar 
    21.Corre, N., Bouchart, V., Ourry, A. & Boucaud, J. Mobilization of nitrogen reserves during regrowth of defoliated Trifolium repens L. and identification of potential vegetative storage proteins. J. Exp. Bot. 47, 1111–1118 (1996).CAS 
    Article 

    Google Scholar 
    22.Granstedt, R. C. & Huffaker, R. C. Identification of the leaf vacuole as a major nitrate storage pool. Plant Physiol. 70, 410–413 (1982).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Dong, B. C. et al. How internode length, position and presence of leaves affect survival and growth of Alternanthera philoxeroides after fragmentation?. Evol. Ecol. 24, 1447–1461 (2010).Article 

    Google Scholar 
    24.Wu, Y. J., Du, T. S. & Wang, L. X. Isotope signature of maize stem and leaf and investigation of transpiration and water transport. Agric. Water Manag. 247, 106727. https://doi.org/10.1016/j.agwat.2020.106727 (2021).Article 

    Google Scholar 
    25.Khaitov, B. et al. Licorice (Glycyrrhiza glabra)—Growth and phytochemical compound secretion in degraded lands under drought stress. Sustainability 13, 2923. https://doi.org/10.3390/su13052923 (2021).Article 

    Google Scholar 
    26.Poorter, H., Remkes, C. & Lambers, H. Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol. 94, 621–627 (1990).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Mommer, L. & Visser, E. J. W. Underwater photosynthesis in flooded terrestrial plants: A matter of leaf plasticity. Ann. Bot. Lond. 96, 581–589 (2005).CAS 
    Article 

    Google Scholar 
    28.Gibbs, J. & Greenway, H. Review: Mechanisms of anoxia tolerance in plants I. Growth, survival and anaerobic catabolism. Funct. Plant Biol. 30, 353 (2003).PubMed 
    Article 

    Google Scholar 
    29.Wang, H. F. et al. Survival and growth response of Vetiveria zizanioides, Acorus calamus and Alternanthera philoxeroides to long-term submergence. Acta Ecol. Sinica 28, 2571–2580 (2008).Article 

    Google Scholar 
    30.Singh, H. B., Singh, B. B. & Ram, P. C. Submergence tolerance of rain fed lowland rice: Search for physiological marker traits. J. Plant Physiol. 158, 883–889 (2001).CAS 
    Article 

    Google Scholar 
    31.Das, K. K., Sarkar, R. K. & Ismail, A. M. Elongation ability and nonstructural carbohydrate levels in relation to submergence tolerance in rice. Plant Sci. 168, 131–136 (2005).CAS 
    Article 

    Google Scholar 
    32.Laan, P. & Blom, C. W. P. M. Growth and survival responses of Rumex species to flooded and submerged conditions: The importance of shoot elongation, underwater photosynthesis and reserve carbohydrates. J. Exp. Bot. 228, 775–783 (1990).Article 

    Google Scholar 
    33.Lynn, D. E. & Waldren, S. Survival of Ranunculus repens L. (Creeping Buttercup) in an amphibious habitat. Ann. Bot. Lond. 91, 75–84 (2003).CAS 
    Article 

    Google Scholar 
    34.Kende, H., van deer Knaap, E. & Cho, H. T. Deep water rice: A model plant to study stem elongation. Plant Physiol. 118, 1105–1110 (1998).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Voesenek, L. A. C. J. et al. Plant hormones regulate fast shoot elongation under water: From genes to communities. Ecology 85, 16–27 (2003).Article 

    Google Scholar 
    36.Voesenek, L. A. C. J. et al. How plants cope with complete submergence. New Phytol. 170, 213–226 (2006).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Groeneveld, H. W. & Voesenek, L. A. C. J. Submergence-induced petiole elongation in Rumex palustris is controlled by developmental stage and storage compounds. Plant Soil. 253, 115–123 (2003).CAS 
    Article 

    Google Scholar 
    38.Jackson, M. B. & Colmer, T. D. Response and adaptation by plants to flooding stress. Ann. Bot. Lond. 96, 501–505 (2005).CAS 
    Article 

    Google Scholar 
    39.Banach, K. et al. Differences in flooding tolerance between species from two wetland habitats with contrasting hydrology: Implications for vegetation development in future floodwater retention areas. Ann. Bot Lond. 103, 341–351 (2009).Article 

    Google Scholar 
    40.Bailey-Serres, J. & Voesenek, L. A. C. J. Flooding stress: Acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313–339 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Kawano, N., Ito, O. & Sakagami, J. I. Morphological and physiological responses of rice seedlings to complete submergence (flash flooding). Ann. Bot. Lond. 103, 161–169 (2009).Article 

    Google Scholar 
    42.Luo, F. L. et al. Recovery dynamics of growth, photosynthesis and carbohydrate accumulation after de-submergence: A comparison between two wetland plants showing escape and quiescence strategies. Ann. Bot. Lond. 107, 49–63 (2011).CAS 
    Article 

    Google Scholar 
    43.Akman, M. et al. Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibia, Rorippa sylvestris and their hybrid. Ann. Bot. Lond. 109, 1263–1275 (2012).CAS 
    Article 

    Google Scholar 
    44.He, J. B. et al. Survival tactics of Ranunculus species in river floodplains. Oecologia 118, 1–8 (1999).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Julien, M. H., Bourne, A. S. & Low, V. H. K. Growth of the weed Alternanthera philoxeroides (Martius) Grisebach, (alligator weed) in aquatic and terrestrial habitats in Australia. Plant Prot. Q. 7, 102–108 (1992).
    Google Scholar 
    46.Mauchamp, A., Blanch, S. & Grillas, P. Effects of submergence on the growth of Phragmites australis seedlings. Aquat. Bot. 69, 147–164 (2001).Article 

    Google Scholar 
    47.Chen, H. J., Qualls, R. G. & Miller, G. C. Adaptive responses of Lepidium latifolium to soil flooding: Biomass allocation, adventitious rooting, aerenchyma formation and ethylene production. Environ. Exp. Bot. 48, 119–128 (2002).Article 

    Google Scholar 
    48.Shen, J. Y., Shen, M. Q., Wang, X. H. & Lu, Y. T. Effect of environmental factors on shoot emergence and vegetative growth of alligatrorweed (Alternanthera philoxeroides). Weed Sci. 53, 471–478 (2005).CAS 
    Article 

    Google Scholar 
    49.Schooler, S. S. Alternanthera philoxeroides (Martius) Grisebach. A Handbook of Global Freshwater Invasive Species (ed. Francis, R. A.) 25–35 (Earthscan, 2012).50.Blom, C. W. P. M. & Voesenek, L. A. C. J. Flooding: The survival strategies of plants. Trends Ecol. Evol. 11, 290–295 (1996).CAS 
    PubMed 
    Article 

    Google Scholar 
    51.Vartapetian, B. B. & Jackson, M. B. Plant adaptations to anaerobic stress. Ann. Bot-London 79, 3–20 (1997).CAS 
    Article 

    Google Scholar 
    52.Visser, E. J. W., Bögemann, G. M., Van De Steeg, H. M., Pierik, R. & Blom, C. W. P. M. Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation. New Phytol. 148, 93–103 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Ruprecht, E., Fenesi, A. & Nijs, I. Are plasticity in functional traits and constancy in performance traits linked with invasiveness? An experimental test comparing invasive and naturalized plant species. Biol. Invasions 16, 1359–1372 (2014).Article 

    Google Scholar 
    54.Poorter, H. et al. Biomass allocation to leaves, stems and roots: Meta-analyses of interspecific variation and environmental control. New Phytol. 193, 30–50 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    55.Fu, H. et al. An alternative mechanism for shade adaptation: Implication of allometric responses of three submersed macrophytes to water depth. Ecol. Res. 27, 1087–1094 (2012).Article 

    Google Scholar 
    56.The weather network. https://www.tianqi.com/ More

  • in

    First come, first served: superinfection exclusion in Deformed wing virus is dependent upon sequence identity and not the order of virus acquisition

    1.Honey: market value worldwide 2007–2016. https://www.statista.com/statistics/933928/global-market-value-of-honey/. Accessed Nov 2020.2.Highfield AC, El Nagar A, Mackinder LCM, Noël LM-LJ, Hall MJ, Martin SJ, et al. Deformed wing virus implicated in overwintering honeybee colony losses. Appl Environ Microbiol. 2009;75:7212–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    3.Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol. 2004;85:3747–55.CAS 
    PubMed 

    Google Scholar 
    4.Lanzi G, Miranda JRD, Boniotti MB, Cameron CE, Lavazza A, Capucci L, et al. Molecular and biological characterization of Deformed wing virus of honeybees (Apis mellifera L.). J Virol. 2006;80:4998–5009.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    5.Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T, Nomoto A, et al. Kakugo virus from brains of aggressive worker honeybees. Adv Virus Res. 2005;65:1–27.CAS 
    PubMed 

    Google Scholar 
    6.Dalmon A, Desbiez C, Coulon M, Thomasson M, Le Conte Y, Alaux C, et al. Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV). Sci Rep. 2017;7:41045.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    7.Zioni N, Soroker V, Chejanovsky N. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology. 2011;417:106–12.CAS 
    PubMed 

    Google Scholar 
    8.Ryabov EV, Childers AK, Chen Y, Madella S, Nessa A, Vanengelsdorp D, et al. Recent spread of Varroa destructor virus – 1, a honey bee pathogen, in the United States. Sci Rep. 2017;7:17447.PubMed 
    PubMed Central 

    Google Scholar 
    9.Moore J, Jironkin A, Chandler D, Burroughs N, Evans DJ, Ryabov EV. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J Gen Virol. 2011;92:156–61.CAS 
    PubMed 

    Google Scholar 
    10.Mordecai GJ, Brettell LE, Martin SJ, Dixon D, Jones IM, Schroeder DC. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISME J. 2015;10:1182–91.PubMed 
    PubMed Central 

    Google Scholar 
    11.Woodford L, Evans DJ. Deformed wing virus: using reverse genetics to tackle unanswered questions about the most important viral pathogen of honey bees. FEMS Microbiol Rev. 2020; fuaa070, https://doi.org/10.1093/femsre/fuaa070.12.Mordecai GJ, Wilfert L, Martin SJ, Jones IM, Schroeder DC. Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. ISME J. 2016;10:1264–73.CAS 
    PubMed 

    Google Scholar 
    13.McMahon DP, Natsopoulou ME, Doublet V, Fürst M, Weging S, Brown MJF, et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc Biol Sci. 2016;283:443–9.
    Google Scholar 
    14.Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R, Martin SJM, et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science. 2016;351:594–7.CAS 
    PubMed 

    Google Scholar 
    15.de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol. 2010;103:S48–S61.PubMed 

    Google Scholar 
    16.Roberts JMK, Anderson DL, Durr PA. Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep. 2017;7:6925.PubMed 
    PubMed Central 

    Google Scholar 
    17.Yue C, Schröder M, Gisder S, Genersch E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol. 2007;88:2329–36.CAS 
    PubMed 

    Google Scholar 
    18.Ryabov EV, Childers AK, Lopez D, Grubbs K, Posada-Florez F, Weaver D, et al. Dynamic evolution in the key honey bee pathogen deformed wing virus: novel insights into virulence and competition using reverse genetics. PLoS Biol. 2019; 17; https://doi.org/10.1371/journal.pbio.3000502.19.Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE, Powell M, et al. Global honey bee viral landscape altered by a parasitic mite. Science. 2012;336:1304–6.CAS 
    PubMed 

    Google Scholar 
    20.Loope KJ, Baty JW, Lester PJ, Wilson Rankin EE. Pathogen shifts in a honeybee predator following the arrival of the Varroa mite. Proc Biol Sci. 2019;286:20182499.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC, Chandler D, et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog. 2014;10:e1004230.PubMed 
    PubMed Central 

    Google Scholar 
    22.Kevill JL, de Souza FS, Sharples C, Oliver R, Schroeder DC, Martin SJ. DWV-A lethal to honey bees (Apis mellifera): a colony level survey of DWV variants (A, B, and C) in England, Wales, and 32 States across the US. Viruses. 2019;11:426.PubMed Central 

    Google Scholar 
    23.Tehel A, Vu Q, Bigot D, Gogol-Döring A, Koch P, Jenkins C, et al. The two prevalent genotypes of an emerging infectious disease, Deformed wing virus, cause equally low pupal mortality and equally high wing deformities in host honey bees. Viruses. 2019;11:114.CAS 
    PubMed Central 

    Google Scholar 
    24.Norton AM, Remnant EJ, Buchmann G, Beekman M. Accumulation and competition amongst Deformed wing virus genotypes in naïve Australian honeybees provides insight Into the increasing global prevalence of genotype B. Front Microbiol. 2020;11:620.PubMed 
    PubMed Central 

    Google Scholar 
    25.Gusachenko ON, Woodford L, Balbirnie-Cumming K, Campbell EM, Christie CR, Bowman AS, et al. Green bees: reverse genetic analysis of Deformed wing virus transmission, replication, and tropism. Viruses. 2020;12:532.CAS 
    PubMed Central 

    Google Scholar 
    26.Steck FT, Rubin H. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology. 1966;29:642–53.CAS 
    PubMed 

    Google Scholar 
    27.Adams RH, Brown DT. BHK cells expressing Sindbis virus-induced homologous interference allow the translation of nonstructural genes of superinfecting virus. J Virol. 1985;54:351–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Strauss JH, Strauss EG. The alphaviruses: gene expression, replication, and evolution. Microbiol Rev. 1994;58:491–562.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Karpf AR, Lenches E, Strauss EG, Strauss JH, Brown DT. Superinfection exclusion of alphaviruses in three mosquito cell lines persistently infected with Sindbis virus. J Virol. 1997;71:7119–23.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    30.Singh IR, Suomalainen M, Varadarajan S, Garoff H, Helenius A. Multiple mechanisms for the inhibition of entry and uncoating of superinfecting Semliki Forest virus. Virology. 1997;231:59–71.CAS 
    PubMed 

    Google Scholar 
    31.Geib T, Sauder C, Venturelli S, Hässler C, Staeheli P, Schwemmle M. Selective virus resistance conferred by expression of Borna disease virus nucleocapsid components. J Virol. 2003;77:4283–90.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Edwards MC, Bragg J, Jackson AO. Natural resistance mechanisms to viruses in barley. In: Loebenstein G and Carr JP, editors. Natural Resistance Mechanisms of Plants to Viruses. Dordrecht, The Netherlands: Springer; 2006. p. 465–501.33.Bergua M, Zwart MP, El-Mohtar C, Shilts T, Elena SF, Folimonova SY. A viral protein mediates superinfection exclusion at the whole-organism level but Is not required for exclusion at the cellular Level. J Virol. 2014;88:11327–38.PubMed 
    PubMed Central 

    Google Scholar 
    34.Michel N, Allespach I, Venzke S, Fackler OT, Keppler OT. The Nef protein of human immunodeficiency virus establishes superinfection immunity by a dual strategy to downregulate cell-surface CCR5 and CD4. Curr Biol. 2005;15:714–23.CAS 
    PubMed 

    Google Scholar 
    35.Tscherne DM, Evans MJ, von Hahn T, Jones CT, Stamataki Z, McKeating JA, et al. Superinfection exclusion in cells infected with hepatitis C virus. J Virol. 2007;81:3693–703.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Leonard SP, Powell JE, Perutka J, Geng P, Heckmann LC, Horak RD, et al. Engineered symbionts activate honey bee immunity and limit pathogens. Science. 2020;367:573–6.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    37.Lamp B, Url A, Seitz K, Rgen Eichhorn J, Riedel C, Sinn LJ, et al. Construction and rescue of a molecular clone of Deformed wing virus (DWV). PLoS ONE. 2016;11:e0164639.38.Gusachenko ON, Woodford L, Balbirnie-Cumming K, Ryabov EV, Evans DJ. Evidence for and against deformed wing virus spillover from honey bees to bumble bees: a reverse genetic analysis. Sci Rep. 2020;10:16847.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Routh A, Johnson JE. Discovery of functional genomic motifs in viruses with ViReMa – a Virus Recombination Mapper – for analysis of next-generation sequencing data. Nucleic Acids Res. 2014;42:e11.CAS 
    PubMed 

    Google Scholar 
    40.Ryabov EV, Christmon K, Heerman MC, Posada-Florez F, Harrison RL, Chen Y, et al. Development of a honey bee RNA virus vector based on the genome of a Deformed wing virus. Viruses. 2020;12:374.CAS 
    PubMed Central 

    Google Scholar 
    41.Mueller S, Wimmer E. Expression of foreign proteins by poliovirus polyprotein fusion: analysis of genetic stability reveals rapid deletions and formation of cardioviruslike open reading frames. J Virol. 1998;72:20–31.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell. 1986;47:433–43.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Egger D, Bienz K. Recombination of poliovirus RNA proceeds in mixed replication complexes originating from distinct replication start sites. J Virol. 2002;76:10960–71.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Lowry K, Woodman A, Cook J, Evans DJ. Recombination in enteroviruses is a biphasic replicative process involving the generation of greater-than genome length ‘imprecise’ Intermediates. PLoS Pathog. 2014;10; https://doi.org/10.1371/journal.ppat.1004191.45.de Miranda JR, Fries I. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol. 2008;98:184–9.PubMed 

    Google Scholar 
    46.Yañez O, Jaffé R, Jarosch A, Fries I, Robin FAM, Robert JP, et al. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): Implications for sexual transmission of a major honey bee virus. Apidologie. 2012;43:17–30.
    Google Scholar 
    47.Simon KO, Cardamone JJ Jr, Whitaker-Dowling PA, Youngner JS, Widnell CC. Cellular mechanisms in the superinfection exclusion of vesicular stomatitis virus. Virology. 1990;177:375–9.CAS 
    PubMed 

    Google Scholar 
    48.Stevenson M, Meier C, Mann AM, Chapman N, Wasiak A. Envelope glycoprotein of HIV induces interference and cytolysis resistance in CD4+ cells: mechanism for persistence in AIDS. Cell. 1988;53:483–96.CAS 
    PubMed 

    Google Scholar 
    49.Bratt MA, Rubin H.Specific interference among strains of Newcastle disease virus. II. Comparison of interference by active and inactive virus.Virology. 1968;35:381–94.CAS 
    PubMed 

    Google Scholar 
    50.Zou G, Zhang B, Lim P-Y, Yuan Z, Bernard KA, Shi P-Y. Exclusion of West Nile virus superinfection through RNA replication. J Virol. 2009;83:11765–76.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    51.Ziebell H, Carr JP. Cross-protection: a century of mystery. Adv Virus Res. 2010;76:211–64.CAS 
    PubMed 

    Google Scholar 
    52.Folimonova SY. Developing an understanding of cross-protection by Citrus tristeza virus. Front Microbiol. 2013;4; https://doi.org/10.3389/fmicb.2013.00076.53.Gisder S, Genersch E. Direct evidence for infection of mites with the bee-pathogenic Deformed wing virus variant B – but not variant A – via fluorescence-hybridization analysis. J Virol. 2021;95:e01786–20.CAS 

    Google Scholar 
    54.Posada-Florez F, Childers AK, Heerman MC, Egekwu NI, Cook SC, Chen Y, et al. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci Rep. 2019;9:12445.PubMed 
    PubMed Central 

    Google Scholar 
    55.Barr JN, Fearns R. How RNA viruses maintain their genome integrity. J Gen Virol. 2010;91:1373–87.CAS 
    PubMed 

    Google Scholar 
    56.Bentley K, Evans DJ. Mechanisms and consequences of positive-strand RNA virus recombination. J Gen Virol. 2018;99:1345–56.CAS 
    PubMed 

    Google Scholar 
    57.Muslin C, Mac Kain A, Bessaud M, Blondel B, Delpeyroux F. Recombination in enteroviruses, a multi-step modular evolutionary process. Viruses. 2019;11:859.CAS 
    PubMed Central 

    Google Scholar 
    58.Alnaji FG, Bentley K, Pearson A, Woodman A, Moore JD, Fox H, et al. Recombination in enteroviruses is a ubiquitous event independent of sequence homology and RNA structure. 2020; preprint at bioRxiv; https://doi.org/10.1101/2020.09.29.319285.59.Brutscher LM, Flenniken ML. RNAi and antiviral defense in the honey bee. J Immunol Res. 2015;2015:941897.PubMed 
    PubMed Central 

    Google Scholar 
    60.Chejanovsky N, Ophir R, Schwager MS, Slabezki Y, Grossman S, Cox-Foster D. Characterization of viral siRNA populations in honey bee colony collapse disorder. Virology. 2014;454-5:176–83.
    Google Scholar 
    61.Desai SD, Eu YJ, Whyard S, Currie RW. Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion. Insect Mol Biol. 2012;21:446–55.CAS 
    PubMed 

    Google Scholar 
    62.Hunter W, Ellis J, Vanengelsdorp D, Hayes J, Westervelt D, Glick E, et al. Large-scale field application of RNAi technology reducing Israeli acute paralysis virus disease in honey bees (Apis mellifera, hymenoptera: Apidae). PLoS Pathog. 2010;6:e1001160.PubMed 
    PubMed Central 

    Google Scholar 
    63.Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E, et al. IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol Biol. 2009;18:55–60.CAS 
    PubMed 

    Google Scholar  More

  • in

    Behavior and body size modulate the defense of toxin-containing sawfly larvae against ants

    1.Evans, D. L. & Schmidt, J. O. Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators (State University of New York Press, Albany, 1990).
    Google Scholar 
    2.Callow, L. L. Sawfly poisoning in cattle. Queensl. Agric. J. 81, 155–161 (1955).
    Google Scholar 
    3.Oelrichs, P. B., MacLeod, J. K. & Williams, D. H. Lophyrotomin a new hepatotoxic octapeptide from sawfly larvae Lophyrotoma interrupta. Toxicon 21(Suppl.3), 321–323 (1983).Article 

    Google Scholar 
    4.Oelrichs, P. B. et al. Unique toxic peptides isolated from sawfly larvae in three continents. Toxicon 37, 537–544 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Dutra, F., Riet-Correa, F., Mendez, M. C. & Paiva, N. Poisoning of cattle and sheep in Uruguay by sawfly (Perreyia flavipes) larvae. Vet. Hum. Toxicol. 39, 281–286 (1997).CAS 
    PubMed 

    Google Scholar 
    6.Kannan, R., Oelrichs, P. B., Thamsborg, S. M. & Williams, D. H. Identification of the octapeptide lophyrotomin in the European birch sawfly (Arge pullata). Toxicon 26, 224–226 (1988).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Tessele, B., Brum, J. S., Schild, A. L., Soares, M. P. & Barros, C. S. L. Sawfly larval poisoning in cattle: Report on new outbreaks and brief review of the literature. Pesqui. Vet. Bras. 32, 1095–1102 (2012).Article 

    Google Scholar 
    8.Wouters, A. T. B. et al. Brain lesions associated with acute toxic hepatopathy in cattle. J. Vet. Diagn. Investig. 29, 287–292 (2017).Article 

    Google Scholar 
    9.Boevé, J.-L., Rozenberg, R., Shinohara, A. & Schmidt, S. Toxic peptides occur frequently in pergid and argid sawfly larvae. PLoS One 9(8), e105301 (2014).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    10.Boevé, J.-L., Nyman, T., Shinohara, A. & Schmidt, S. Endogenous toxins and the coupling of gregariousness to conspicuousness in Argidae and Pergidae sawflies. Sci. Rep. 8, 17636 (2018).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    11.Boevé, J.-L. & Rozenberg, R. Body distribution of toxic peptides in larvae of a pergid and an argid sawfly species. Sci. Nat. 107, 1 (2020).Article 
    CAS 

    Google Scholar 
    12.Maxwell, D. E. The comparative internal larval anatomy of sawflies (Hymenoptera: Symphyta). Can. Entomol. 87, 1–132 (1955).Article 

    Google Scholar 
    13.Morrow, P. A., Bellas, T. E. & Eisner, T. Eucalyptus oils in the defensive oral discharge of Australian sawfly larvae (Hymenoptera: Pergidae). Oecologia 24, 193–206 (1976).CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 
    14.Schmidt, S., McKinnon, A. E., Moore, C. J. & Walter, G. H. Chemical detoxification vs mechanical removal of host plant toxins in Eucalyptus feeding sawfly larvae (Hymenoptera: Pergidae). J. Insect Physiol. 56, 1770–1776 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Lorenz, H. & Kraus, M. Die Larvalsystematik der Blattwespen (Tenthredinoidea und Megalodontoidea) (Akademie-Verlag, Berlin, 1957).
    Google Scholar 
    16.Schmidt, S., Walter, G. H., Grigg, J. & Moore, C. J. Sexual communication and host plant associations of Australian pergid sawflies (Hymenoptera: Symphyta: Pergidae). In Recent Sawfly Research: Synthesis and Prospects (eds Blank, S. M. et al.) 173–193 (Goecke & Evers, Krefeld, 2006).
    Google Scholar 
    17.Petre, C.-A., Detrain, C. & Boevé, J.-L. Anti-predator defence mechanisms in sawfly larvae of Arge (Hymenoptera, Argidae). J. Insect Physiol. 53, 668–675 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Boevé, J.-L., Marín-Armijos, D. S., Domínguez, D. F. & Smith, D. R. Sawflies (Hymenoptera: Argidae, Pergidae, Tenthredinidae) from southern Ecuador, with a new record for the country and some ecological data. J. Hymenopt. Res. 51, 55–89 (2016).Article 

    Google Scholar 
    19.Shinohara, A., Hara, H. & Kim, J. The species-group of Arge captiva (Insecta, Hymenoptera, Argidae). Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 35, 249–278 (2009).
    Google Scholar 
    20.Hara, H. & Shinohara, A. Arge enkianthus n. sp. (Hymenoptera, Argidae) feeding on Enkianthus campanulatus in Japan. Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 38, 21–32 (2012).
    Google Scholar 
    21.Shinohara, A., Kojima, H. & Hara, H. New host plant records and life history notes on Spinarge flavicostalis (Hymenoptera: Argidae) in Japan. Bull. Natl. Museum Nat. Sci. Ser. A (Zoology) Tokyo 39, 185–191 (2013).
    Google Scholar 
    22.Ruxton, G. D., Sherratt, T. N. & Speed, M. P. Avoiding Attack. The Evolutionary Ecology of Crypsis, Warning Signals, and Mimicry (Oxford University Press, Oxford, 2004).Book 

    Google Scholar 
    23.Boevé, J.-L., Blank, S. M., Meijer, G. & Nyman, T. Invertebrate and avian predators as drivers of chemical defensive strategies in tenthredinid sawflies. BMC Evol. Biol. 13, 198 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Benson, R. B. An introduction to the natural history of British sawflies. Trans. Soc. Br. Entomol. 10, 45–142 (1950).
    Google Scholar 
    25.Codella, S. G. & Raffa, K. F. Defense strategies of folivorous sawflies. In Sawfly Life History Adaptations to Woody Plants (eds Wagner, M. & Raffa, K. F.) 261–294 (Academic Press, Cambridge, 1993).
    Google Scholar 
    26.Schwerdtfeger, F. Untersuchungen über die Wirkung von Ameisen-Ansiedlungen auf die Dichte der Kleinen Fichtenblattwespe. Z. Angew. Entomol. 66, 187–206 (1970).
    Google Scholar 
    27.Woodman, R. L. & Price, P. W. Differential larval predation by ants can influence willow sawfly community structure. Ecology 73, 1028–1037 (1992).Article 

    Google Scholar 
    28.Boevé, J.-L. & Schaffner, U. Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134, 104–111 (2003).PubMed 
    Article 
    ADS 

    Google Scholar 
    29.Dettner, K. Toxins, defensive compounds and drugs from insects. In Insect Molecular Biology and Ecology (ed. Hoffmann, K. H.) 39–93 (Taylor & Francis, Boca Raton, 2015).
    Google Scholar 
    30.Taeger, A., Blank, S. M. & Liston, A. D. World Catalog of Symphyta (Hymenoptera). Zootaxa 2580, 1–1064 (2010).Article 

    Google Scholar 
    31.Boevé, J.-L. & Rozenberg, R. Berberis sawfly contains toxic peptides not only at larval stage. Sci. Nat. 106, 14 (2019).Article 
    CAS 

    Google Scholar 
    32.Schoenly, K. The predators of insects. Ecol. Entomol. 15, 333–345 (1990).Article 

    Google Scholar 
    33.Way, M. J. & Khoo, K. C. Role of ants in pest managment. Annu. Rev. Entomol. 37, 479–503 (1992).Article 

    Google Scholar 
    34.Dyer, L. A. A quantification of predation rates, indirect positive effects on plants, and foraging variation of the giant tropical ant, Paraponera clavata. J. Insect Sci. 2, 18 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Jervis, M. & Kidd, N. Insect Natural Enemies. Practical Approaches to their Study and Evaluation (Chapman & Hall, London, 1996).Book 

    Google Scholar 
    36.Philpott, S. M., Greenberg, R., Bichier, P. & Perfecto, I. Impacts of major predators on tropical agroforest arthropods: Comparisons within and across taxa. Oecologia 140, 140–149 (2004).PubMed 
    Article 
    ADS 

    Google Scholar 
    37.Rosumek, F. B. et al. Ants on plants: A meta-analysis of the role of ants as plant biotic defenses. Oecologia 160, 537–549 (2009).PubMed 
    Article 
    ADS 
    PubMed Central 

    Google Scholar 
    38.Fittkau, E. J. & Klinge, H. On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica 5, 2–14 (1973).Article 

    Google Scholar 
    39.Hölldobler, B. & Wilson, E. O. The Ants (Harvard University Press, Harvard, 1990).Book 

    Google Scholar 
    40.Ryder Wilkie, K. T., Mertl, A. L. & Traniello, J. F. A. Species diversity and distribution patterns of the ants of Amazonian Ecuador. PLoS One 5, e13146 (2010).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    41.Wills, B. D. & Landis, D. A. The role of ants in north temperate grasslands: A review. Oecologia 186, 323–338 (2018).CAS 
    PubMed 
    Article 
    ADS 

    Google Scholar 
    42.Pasteels, J. M., Grégoire, J.-C. & Rowell-Rahier, M. The chemical ecology of defense in arthropods. Annu. Rev. Entomol. 28, 263–289 (1983).CAS 
    Article 

    Google Scholar 
    43.Whitman, D. W., Blum, M. R. & Alsop, D. W. Allomones: Chemicals for defense. In Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators (eds Evans, D. L. & Schmidt, J. O.) 289–351 (State University of New York Press, Albany, 1990).
    Google Scholar 
    44.Eisner, T., Eisner, M. & Siegler, M. Secret Weapons: Defenses of Insects, Spiders, Scorpions, and other Many-Legged Creatures (Harvard University Press, Harvard, 2005).
    Google Scholar 
    45.Morton, T. C. & Vencl, F. V. Larval beetles form a defense from recycled host-plant chemicals discharged as fecal wastes. J. Chem. Ecol. 24, 765–785 (1998).CAS 
    Article 

    Google Scholar 
    46.Zhang, S. et al. A novel property of spider silk: Chemical defence against ants. Proc. R. Soc. B Biol. Sci. 279, 1824–1830 (2011).Article 
    CAS 

    Google Scholar 
    47.Hilker, M. Protective devices of early developmental stages in Pyrrhalta viburni (Coleoptera, Chrysomelidae). Oecologia 92, 71–75 (1992).PubMed 
    Article 
    ADS 
    PubMed Central 

    Google Scholar 
    48.Gross, J., Eben, A., Müller, I. & Wensing, A. A well protected intruder: The effective antimicrobial defense of the invasive ladybird Harmonia axyridis. J. Chem. Ecol. 36, 1180–1188 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Gentry, G. L. & Dyer, L. A. On the conditional nature of Neotropical caterpillar defenses against their natural enemies. Ecology 83, 3108–3119 (2009).Article 

    Google Scholar 
    50.Rojas, B. et al. How to fight multiple enemies: Target-specific chemical defences in an aposematic moth. Proc. R. Soc. B Biol. Sci. 284, 20171424 (2017).Article 

    Google Scholar 
    51.Boevé, J.-L. & Pasteels, J. M. Modes of defense in nematine sawfly larvae. Efficiency against ants and birds. J. Chem. Ecol. 11, 1019–1036 (1985).PubMed 
    Article 

    Google Scholar 
    52.Schaffner, U., Boevé, J.-L., Gfeller, H. & Schlunegger, U. P. Sequestration of Veratrum alkaloids by specialist Rhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) and its ecoethological implications. J. Chem. Ecol. 20, 3233–3250 (1994).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Boevé, J.-L. Some sawfly larvae survive predator-prey interactions with pentatomid Picromerus bidens. Sci. Nat. 108, 8 (2021).Article 
    CAS 

    Google Scholar 
    54.Remmel, T., Davison, J. & Tammaru, T. Quantifying predation on folivorous insect larvae: The perspective of life-history evolution. Biol. J. Linn. Soc. 104, 1–18 (2011).Article 

    Google Scholar 
    55.Verhaagh, M. „Parasitierung” einer Ameisen-Pflanzen-Symbiose in neotropischen Regenwald? Carolinea 46, 150 (1988).
    Google Scholar 
    56.Boevé, J.-L. & Heilporn, S. Secretion of the ventral glands in Craesus sawfly larvae. Biochem. Syst. Ecol. 36, 836–841 (2008).Article 
    CAS 

    Google Scholar 
    57.Aili, S. R. et al. Diversity of peptide toxins from stinging ant venoms. Toxicon 92, 166–178 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Boevé, J.-L. & Müller, C. Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators. Chemoecology 15, 51–58 (2005).Article 
    CAS 

    Google Scholar 
    59.Chevin, H. Notes sur les Hyménoptères Tenthredoides. 2. Identification des larves d’Arge pagana (Panz.) et d’Arge ochropa (Gmel.). Bull. Mens. la Société Linnéenne Lyon 1, 2–5 (1972).Article 

    Google Scholar 
    60.Schmidt, S. & Smith, D. R. Pergidae of the World – An online catalogue of the sawfly family Pergidae (Insecta, Hymenoptera, Symphyta). World Wide Web electronic publication (2018). Available at: http://pergidae.snsb-zsm.de. (Accessed: 25th July 2016)61.Olofsson, E. Predation by Formica polyctena Förster (Hym., Formicidae) on newly emerged larvae of Neodiprion sertifer (Geoffroy) (Hym., Diprionidae). J. Appl. Entomol. 114, 315–319 (1992).Article 

    Google Scholar 
    62.Hughes, L., Westoby, M. & Jurado, E. Convergence of elaiosomes and insect prey: Evidence from ant foraging behaviour and fatty acid composition. Funct. Ecol. 8, 358–365 (1994).Article 

    Google Scholar  More

  • in

    Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: the effect of temperature

    1.Van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J. & Urbaneja, A. biological control using invertebrates and microorganisms: Plenty of new opportunities. Biocontrol 63, 39–59 (2018).Article 

    Google Scholar 
    2.Koch, R. The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 3, 1–16 (2003).Article 

    Google Scholar 
    3.Huang, N.-X. et al. Long-term, large-scale releases of Trichogramma promote pesticide decrease in maize in northeastern China. Entomol. Gen. 40, 331–335 (2020).Article 

    Google Scholar 
    4.Gibert, J. P. Temperature directly and indirectly influences food web structure. Sci. Rep. 9, 1–8 (2019).CAS 
    Article 

    Google Scholar 
    5.Wootton, J. T. & Emmerson, M. Measurement of interaction strength in nature. Annu. Rev. Ecol. Evol. Syst. 36, 419–444 (2005).Article 

    Google Scholar 
    6.Novak, M. & Wootton, J. T. Using experimental indices to quantify the strength of species interactions. Oikos 119, 1057–1063 (2010).Article 

    Google Scholar 
    7.Holling, C. S. Some characteristics of simple types of predation and parasitism. Can. Entomol. 91, 385–398 (1959).Article 

    Google Scholar 
    8.Fathipour, Y., Maleknia, B., Bagheri, A., Soufbaf, M. & Reddy, G. V. Functional and numerical responses, mutual interference, and resource switching of Amblyseius swirskii on two-spotted spider mite. Biol. Control 146, 104266 (2020).CAS 
    Article 

    Google Scholar 
    9.Van Lenteren, J. C. et al. Pest kill rate as aggregate evaluation criterion to rank biological control agents: A case study with Neotropical predators of Tuta absoluta on tomato. Bull. Entomol. Res. 109, 812–820 (2019).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    10.Xia, P.-L., Yu, X.-L., Li, Z.-T. & Feng, Y. The impacts of Harmonia axyridis cues on foraging behavior of Aphidius gifuensis to Myzus persicae. J. Asia Pac. Entomol. 24, 278–284 (2021).Article 

    Google Scholar 
    11.Juliano, S. A. Non-linear curve fitting: Predation and functional response curve. Design and analysis of ecological experiment (eds Scheiner, S.M. & Gurevitch, J.), 178–196. (Chapman and Hall, London, 2001).12.Jeschke, J. M. & Tollrian, R. Effects of predator confusion on functional responses. Oikos 111, 547–555 (2005).Article 

    Google Scholar 
    13.Pervez, A. Functional responses of coccinellid predators: An illustration of a logistic approach. J. Insect Sci. 5, 5 (2005).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Uiterwaal, S. F. & DeLong, J. P. Multiple factors, including arena size, shape the functional responses of ladybird beetles. J. Appl. Ecol. 55, 2429–2438 (2018).CAS 
    Article 

    Google Scholar 
    15.Parajulee, M., Shrestha, R., Leser, J., Wester, D. & Blanco, C. Evaluation of the functional response of selected arthropod predators on bollworm eggs in the laboratory and effect of temperature on their predation efficiency. Environ. Entomol. 35, 379–386 (2006).Article 

    Google Scholar 
    16.Forster, J. & Hirst, A. G. The temperature-size rule emerges from ontogenetic differences between growth and development rates. Funct. Ecol. 26, 483–492 (2012).Article 

    Google Scholar 
    17.Diamond, S. E. Contemporary climate-driven range shifts: Putting evolution back on the table. Funct. Ecol. 32, 1652–1665 (2018).Article 

    Google Scholar 
    18.Andrew, N. R. et al. Assessing insect responses to climate change: What are we testing for? Where should we be heading?. PeerJ 1, e11 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Jalali, M. A., Tirry, L. & De Clercq, P. Effect of temperature on the functional response of Adalia bipunctata to Myzus persicae. Biocontrol 55, 261–269 (2010).Article 

    Google Scholar 
    20.Moezipour, M., Kafil, M. & Allahyari, H. Functional response of Trichogramma brassicae at different temperatures and relative humidities. Bull. Insectol. 61, 245–250 (2008).
    Google Scholar 
    21.Effect of temperature. Clercq, D. Functional response of the predators Podisus maculiventris (Say) and Podisus nigrispinus (Dallas)(Het., Pentatomidae) to the beet armyworm, Spodoptera exigua (Hübner) (Lep., Noctuidae). J. Appl. Entomol. 125, 131–134 (2001).Article 

    Google Scholar 
    22.Da Silva Nunes, G. et al. Temperature-dependent functional response of Euborellia annulipes (Dermaptera: Anisolabididae) preying on Plutella xylostella (Lepidoptera: Plutellidae) larvae. J. Therm. Biol. 93, 102686 (2020).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    23.Işikber, A. A. Functional response of two coccinellid predators, Scymnus levaillanti and Cycloneda sanguinea, to the cotton aphid, Aphis gossypii. Turk. J. Agric. For. 29, 347–355 (2005).
    Google Scholar 
    24.Walker, R., Wilder, S. M. & González, A. L. Temperature dependency of predation: Increased killing rates and prey mass consumption by predators with warming. Ecol. Evol. 10, 9696–9706 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Davidson, A. T., Hamman, E. A., McCoy, M. W. & Vonesh, J. R. Asymmetrical effects of temperature on stage-structured predator–prey interactions. Funct. Ecol. 35, 1041–1054 (2021).Article 

    Google Scholar 
    26.Murrell, E. G. & Barton, B. T. Warming alters prey density and biological control in conventional and organic agricultural systems. Integr. Comp. Biol. 57, 1–13 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Damien, M. & Tougeron, K. Prey–predator phenological mismatch under climate change. Curr. Opin. Insect. Sci. 35, 60–68 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Daugaard, U., Petchey, O. L. & Pennekamp, F. Warming can destabilize predator–prey interactions by shifting the functional response from Type III to Type II. J. Anim. Ecol. 88, 1575–1586 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Thomas, C. A list of the species of the tribe Aphidini, family Aphidae, found in the United States, which have been heretofore named, with descriptions of some new species. Bull. Ill. Nat. Hist. Surv. 1, 3–16 (1878).Article 

    Google Scholar 
    30.Elbakidze, L., Lu, L. & Eigenbrode, S. Evaluating vector-virus-yield interactions for peas and lentils under climatic variability: A limited dependent variable analysis. J. Agric. Resour. Econ. 36, 504–520 (2011).
    Google Scholar 
    31.Aznar-Fernández, T., Cimmino, A., Masi, M., Rubiales, D. & Evidente, A. Antifeedant activity of long-chain alcohols, and fungal and plant metabolites against pea aphid (Acyrthosiphon pisum) as potential biocontrol strategy. Nat. Prod. Res. 33, 2471–2479 (2019).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    32.Holman, J. Host Plant Catalogue of Aphids (Springer, Berlin, 2009).Book 

    Google Scholar 
    33.Sandhi, R. K. & Reddy, G. V. Biology, ecology, and management strategies for pea aphid (Hemiptera: Aphididae) in pulse crops. J. Integr. Pest Manag. 11, 18 (2020).Article 

    Google Scholar 
    34.Anuj, B. Efficacy and economics of some insecticides and a neem formulation on incidence of pea aphid (Acyrthosiphum pisum) on pea, Pisum sativum. Ann. Plant. Protect. Sci. 4, 131–133 (1996).
    Google Scholar 
    35.Slusher, E. K., Cottrell, T. & Acebes-Doria, A. L. Effects of aphicides on pecan aphids and their parasitoids in pecan orchards. Insects 12, 241 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Soleimani, S. & Madadi, H. Seasonal dynamics of: The pea aphid, Acyrthosiphon pisum (Harris), its natural enemies the seven spotted lady beetle Coccinella septempunctata Linnaeus and variegated lady beetle Hippodamia variegata Goeze, and their parasitoid Dinocampus coccinellae (Schrank). J. Plant Prot. Res. 55, 2015 (2015).Article 
    CAS 

    Google Scholar 
    37.Roy, H. E. et al. The harlequin ladybird, Harmonia axyridis: Global perspectives on invasion history and ecology. Biol. Invasions 18, 997–1044 (2016).Article 

    Google Scholar 
    38.Roy, H., Brown, P. & Majerus, M. In: An ecological and societal approach to biological control (eds. Hokkanen H and Eilenberg J) 295–309 (Kluwer Academic Publishers), Springer, (2006).39.Rasheed, M. A. et al. Lethal and sublethal effects of chlorpyrifos on biological traits and feeding of the aphidophagous predator Harmonia axyridis. Insects 11, 491 (2020).PubMed Central 
    Article 

    Google Scholar 
    40.Gao, G., Liu, S., Feng, L., Wang, Y. & Lu, Z. Effect of temperature on predation by Harmonia axyridis (Pall.)(Coleoptera: Coccinellidae) on the walnut aphids Chromaphis juglandicola Kalt. and Panaphis juglandis (Goeze). Egypt. J. Biol. Pest Control 30, 1–6 (2020).Article 

    Google Scholar 
    41.Islam, Y. et al. Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11, 583 (2020).PubMed Central 
    Article 

    Google Scholar 
    42.Ge, Y. et al. Different predation capacities and mechanisms of Harmonia axyridis (Coleoptera: Coccinellidae) on two morphotypes of pear psylla Cacopsylla chinensis (Hemiptera: Psyllidae). PLoS ONE 14, e0215834 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Ünlü, A. G., Terlau, J. F. & Bucher, R. Predation and avoidance behavior of the pea aphid Acyrthosiphon pisum confronted with native and invasive lady beetles in Europe. Biol. Invasions 2020, 1–10 (2020).
    Google Scholar 
    44.Shah, M. A. & Khan, A. Functional response-a function of predator and prey species. The Bioscan 8, 751–758 (2013).
    Google Scholar 
    45.Moradi, M., Hassanpour, M., Fathi, S. A. A. & Golizadeh, A. Foraging behaviour of Scymnus syriacus (Coleoptera: Coccinellidae) provided with Aphis spiraecola and Aphis gossypii (Hemiptera: Aphididae) as prey: Functional response and prey preference. Eur. J. Entomol. 117, 83–92 (2020).Article 

    Google Scholar 
    46.Sinclair, B. J., Williams, C. M. & Terblanche, J. S. Variation in thermal performance among insect populations. Physiol. Biochem. Zool. 85, 594–606 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Noman, Q. M., Shah, F. M., Mahmood, K. & Razaq, M. Population dynamics of Tephritid fruit flies in citrus and mango orchards of Multan, Southern Punjab, Pakistan. https://doi.org/10.17582/journal.pjz/20191021181023 (2021).48.Logan, J. D., Wolesensky, W. & Joern, A. Temperature-dependent phenology and predation in arthropod systems. Ecol. modell. 196, 471–482 (2006).Article 

    Google Scholar 
    49.Uiterwaal, S. F. & DeLong, J. P. Functional responses are maximized at intermediate temperatures. Ecology 101, e02975 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Wale, M., Jembere, B. & Seyoum, E. Biology of the pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) on cool-season legumes. Int. J. Trop. Insect. Sci. 20, 171–180 (2000).Article 

    Google Scholar 
    51.Seyfollahi, F., Esfandiari, M., Mossadegh, M. & Rasekh, A. Functional response of Hyperaspis polita (Coleoptera, Coccinellidae) to the recently invaded mealybug Phenacoccus solenopsis (Hemiptera, Pseudococcidae). Neotrop. Entomol. 48, 484–495 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Katsarou, I., Margaritopoulos, J. T., Tsitsipis, J. A., Perdikis, D. C. & Zarpas, K. D. Effect of temperature on development, growth and feeding of Coccinella septempunctata and Hippodamia convergens reared on the tobacco aphid, Myzus persicae nicotianae. Biocontrol 50, 565–588 (2005).Article 

    Google Scholar 
    53.Koehler, H. Predatory mites (Gamasina, Mesostigmata). Agric. Ecosyst. Environ. 74, 395–410 (1999).Article 

    Google Scholar 
    54.Farhadi, R., Allahyari, H. & Juliano, S. A. Functional response of larval and adult stages of Hippodamia variegata (Coleoptera: Coccinellidae) to different densities of Aphis fabae (Hemiptera: Aphididae). Environ. Entomol. 39, 1586–1592 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Aqueel, M. & Leather, S. Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids. Ann. Appl. Biol. 160, 6–15 (2012).CAS 
    Article 

    Google Scholar 
    56.Koch, R. L., Hutchison, W. D., Venette, R. & Heimpel, G. E. Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol. Control 28, 265–270 (2003).Article 

    Google Scholar 
    57.He, J., Ma, E., Shen, Y., Chen, W. & Sun, X. Observations of the biological characteristics of Harmonia axyridis (Pallas)(Coleoptera: Coccinellidae). J. Shanghai Agric. College 12, 119–124 (1994).
    Google Scholar 
    58.Huang, Z. et al. Predation and functional response of the multi-coloured Asian ladybeetle Harmonia axyridis on the adult Asian citrus psyllid Diaphorina citri. Biocontrol Sci. Technol. 29, 293–307 (2019).Article 

    Google Scholar 
    59.Lee, J.-H. & Kang, T.-J. Functional response of Harmonia axyridis (Pallas)(Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera: aphididae) in the laboratory. Biol. Control 31, 306–310 (2004).Article 

    Google Scholar 
    60.Xue, Y. et al. Predation by Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Homoptera: Aphididae). Environ. Entomol. 38, 708–714 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Obrycki, J. J. & Kring, T. J. Predaceous Coccinellidae in biological control. Annu. Rev. Entomol. 43, 295–321 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Feng, Y., Zhou, Z.-X., An, M.-R., Yu, X.-L. & Liu, T.-X. The effects of prey distribution and digestion on functional response of Harmonia axyridis (Coleoptera: Coccinellidae). Biol. Control 124, 74–81 (2018).Article 

    Google Scholar 
    63.Dai, C. et al. Can contamination by major systemic insecticides affect the voracity of the harlequin ladybird?. Chemosphere 256, 126986 (2020).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Qin, D. et al. Treating green pea aphids, Myzus persicae, with azadirachtin affects the predatory ability and protective enzyme activity of harlequin ladybirds. Harmonia axyridis. Ecotoxicol. Environ. Saf. 212, 111984 (2021).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Shah, F. M., Razaq, M., Ali, A., Han, P. & Chen, J. Comparative role of neem seed extract, moringa leaf extract and imidacloprid in the management of wheat aphids in relation to yield losses in Pakistan. PLoS ONE 12, e0184639 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    66.Shah, F. M. et al. Action threshold development in cabbage pest management using synthetic and botanical insecticides. Entomol. Gen. 40, 157–172 (2020).Article 

    Google Scholar 
    67.Shah, F. M. et al. Field evaluation of synthetic and neem-derived alternative insecticides in developing action thresholds against cauliflower pests. Sci. Rep. 9, 7684 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    68.Naeem, A. et al. Laboratory induced selection of pyriproxyfen resistance in Oxycarenus hyalinipennis Costa (Hemiptera: Lygaeidae): Cross-resistance potential, realized heritability, and fitness costs determination using age-stage, two-sex life table. Chemosphere 269, 129367. https://doi.org/10.1016/j.chemosphere.122020.129367 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    69.Rix, R. & Cutler, G. Low Doses of a Neonicotinoid stimulate reproduction in a beneficial predatory insect. J. Econ. Entomol. 113, 2179–2186 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    70.Atlıhan, R. & Güldal, H. Prey density-dependent feeding activity and life history of Scymnus subvillosus. Phytoparasitica 37, 35–41 (2009).Article 

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

    Google Scholar 
    72.Vucic-Pestic, O., Ehnes, R. B., Rall, B. C. & Brose, U. Warming up the system: Higher predator feeding rates but lower energetic efficiencies. Glob. Change Biol. 17, 1301–1310 (2011).ADS 
    Article 

    Google Scholar 
    73.Lang, B., Rall, B. C. & Brose, U. Warming effects on consumption and intraspecific interference competition depend on predator metabolism. J. Anim. Ecol. 81, 516–523 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Wu, P., Zhang, J., Haseeb, M., Yan, S. & Kanga, L. Functional responses and intraspecific competition in the ladybird Harmonia axyridis (Coleoptera: Coccinellidae) provided with Melanaphis sacchari (Homoptera: Aphididae) as prey. Eur. J. Entomol. 115, 232–241 (2018).Article 

    Google Scholar 
    75.Hodek, I., van Emden, H. F. & Honěk, A. Diapause/dormancy. Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley Blackwell, Chichester, (2012).76.Li, Y. et al. The effect of different dietary sugars on the development and fecundity of Harmonia axyridis. Front. Physiol. 11, 574851 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Sharma, P., Verma, S., Chandel, R., Shah, M. & Gavkare, O. Functional response of Harmonia dimidiata (fab.) to melon aphid, Aphis gossypii Glover under laboratory conditions. Phytoparasitica 45, 373–379 (2017).Article 

    Google Scholar 
    78.Feng, Y. et al. Conspecific and heterospecific interactions modify the functional response of Harmonia axyridis and Propylea japonica to Aphis citricola. Entomol. Exp. Appl. 166, 873–882 (2018).CAS 
    Article 

    Google Scholar 
    79.Hassanzadeh-Avval, M., Sadeghi-Namaghi, H. & Fekrat, L. Factors influencing functional response, handling time and searching efficiency of Anthocoris minki Dohrn (Hem.: Anthocoridae) as predator of Psyllopsis repens Loginova (Hem.: Psyllidae). Phytoparasitica 47, 341–350 (2019).Article 

    Google Scholar 
    80.Banihashemi, A. S., Seraj, A. A., Yarahmadi, F. & Rajabpour, A. Effect of host plants on predation, prey preference and switching behaviour of Orius albidipennis on Bemisia tabaci and Tetranychus turkestani. Int. J. Trop. Insect Sci. 37, 176–182 (2017).Article 

    Google Scholar 
    81.Abbott, W. S. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265–267 (1925).CAS 
    Article 

    Google Scholar 
    82.R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (2014).83.Rogers, D. Random search and insect population models. J. Anim. Ecol. 41, 369–383 (1972).Article 

    Google Scholar 
    84.Pritchard, D. W., Paterson, R., Bovy, H. C. & Barrios-O’Neill, D. Frair: An R package for fitting and comparing consumer functional responses. Methods Ecol. Evol. 8, 1528–1534 (2017).Article 

    Google Scholar 
    85.Hassell, M. The spatial and temporal dynamics of host-parasitoid interactions (Oxford University Press, 2000).
    Google Scholar  More

  • in

    Tropical deforestation induces thresholds of reproductive viability and habitat suitability in Earth’s largest eagles

    1.McQueen, A. et al. Evolutionary drivers of seasonal plumage colours: colour change by moult correlates with sexual selection, predation risk and seasonality across passerines. Ecol. Lett. 22, 1838–1849 (2019).PubMed 

    Google Scholar 
    2.Menezes, J. F., Kotler, B. P. & Dixon, A. K. Risk pump in Gerbillus pyramidum: quality of poor habitats increases with more conspecifics. Ethol. Ecol. Evol. 31, 140–154 (2019).
    Google Scholar 
    3.Stephens, D., Brown, J. & Ydenberg, R. Foraging: Behavior and Ecology. (University of Chicago Press, 2007).4.Schweiger, A., Fünfstück, H.-J. & Beierkuhnlein, C. Availability of optimal-sized prey affects global distribution patterns of the golden eagle Aquila chrysaetos. J. Avian Biol. 46, 81–88 (2015).
    Google Scholar 
    5.Carbone, C. & Gittleman, J. L. A common rule for the scaling of carnivore density. Science (80-.) 295, 2273–2276 (2002).ADS 
    CAS 

    Google Scholar 
    6.Athreya, V., Odden, M. & Linnell, J. A cat among the dogs: leopard Panthera pardus diet in a human-dominated landscape in western Maharashtra, India. Oryx https://doi.org/10.1017/s0030605314000106 (2014).Article 

    Google Scholar 
    7.Van der Meer, T., McPherson, S. & Downs, C. Temporal changes in prey composition and biomass delivery to African Crowned Eagle nestlings in urban areas of KwaZulu-Natal, South Africa. Ostrich 83, 241–250 (2018).
    Google Scholar 
    8.Miranda, E. B. P., Ribeiro-Jr., R. P. & Strüssmann, C. The ecology of human-anaconda conflict: a study using internet videos. Trop. Conserv. Sci. 9, 26–60 (2016).
    Google Scholar 
    9.Paviolo, A. et al. A biodiversity hotspot losing its top predator: the challenge of jaguar conservation in the Atlantic Forest of South America. Sci. Rep. 6, 37147 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Miranda, E. B. P., Menezes, J. F. S., Farias, C. C., Munn, C. & Peres, C. A. Species distribution modeling reveals strongholds and potential reintroduction areas for the world’s largest eagle. PLoS ONE 14, e0216323 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    11.Marshall, B. M. et al. Hits close to home: repeated persecution of King Cobras (Ophiophagus hannah) in Northeastern Thailand. Trop. Conserv. Sci. 11, 1–14 (2018).
    Google Scholar 
    12.Carbone, C., Pettorelli, N. & Stephens, P. A. The bigger they come, the harder they fall: body size and prey abundance influence predator-prey ratios. Biol. Lett. 7, 312–315 (2011).PubMed 

    Google Scholar 
    13.Garcia-Heras, M. S., Mougeot, F., Simmons, R. E. & Arroyo, B. Regional and temporal variation in diet and provisioning rates suggest weather limits prey availability for an endangered raptor. Ibis (Lond. 1859) 159, 567–579 (2017).
    Google Scholar 
    14.Miranda, E. B., Jácomo, A. T. D. A., Tôrres, N. M., Alves, G. B. & Silveira, L. What are jaguars eating in a half-empty forest? Insights from diet in an overhunted Caatinga reserve. J. Mammal. 99, 724–731 (2018).
    Google Scholar 
    15.Ellis, D. H. & Gombobaatar, S. Ecology of the Golden Eagle in Mongolia, part 2: prey. J. Raptor Res. 54, 30–37 (2020).
    Google Scholar 
    16.Zuluaga, S. & Echeverry-Galvis, M. Á. Domestic fowl in the diet of the Black-and-chestnut Eagle (Spizaetus isidori) in the Eastern Andes of Colombia: a potential conflict with humans. Ornitol. Neotrop. 27, 113–120 (2016).
    Google Scholar 
    17.McPherson, S. C. & Brown, M. Downs CT (2015) Diet of the crowned eagle (Stephanoaetus coronatus) in an urban landscape: potential for human-wildlife conflict?. Urban Ecosyst. https://doi.org/10.1007/s11252-015-0500-6 (2015).Article 

    Google Scholar 
    18.Michalski, F., Boulhosa, R. L. P., Faria, A. & Peres, C. A. Human-wildlife conflicts in a fragmented Amazonian forest landscape: determinants of large felid depredation on livestock. Anim. Conserv. 9, 179–188 (2006).
    Google Scholar 
    19.Lamichhane, B. R. et al. Rapid recovery of tigers Panthera tigris in Parsa Wildlife Reserve, Nepal. Oryx 52, 16–24 (2018).
    Google Scholar 
    20.Tortato, F. R., Izzo, T. J., Hoogesteijn, R. & Peres, C. A. The numbers of the beast: valuation of jaguar (Panthera onca) tourism and cattle depredation in the Brazilian Pantanal. Glob. Ecol. Conserv. 11, 106–114 (2017).
    Google Scholar 
    21.Macdonald, C. et al. Conservation potential of apex predator tourism. Biol. Conserv. 215, 132–141 (2017).
    Google Scholar 
    22.Karanth, K. U., Kumar, N. S., Nichols, J. D., Link, W. A. & Hines, J. E. Tigers and their prey: predicting carnivore densities from prey abundance. Proc. Natl. Acad. Sci. USA 101, 4854–4858 (2004).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Nelson, A. A. et al. Native prey distribution and migration mediates wolf (Canis lupus) predation on domestic livestock in the Greater Yellowstone Ecosystem 94(4). Can. J. Zool. 94, 291–299 (2016).
    Google Scholar 
    24.Terborgh, J. & Estes, J. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature (Island Press, 2013).25.Miranda, E. B. P. Prey composition of harpy eagles (Harpia harpyja) in Raleighvallen, Suriname. Trop. Conserv. Sci. 11, 1–8 (2018).
    Google Scholar 
    26.Miranda, E. B. P. Conservation implications of harpy eagle Harpia harpyja predation patterns. Endanger. Species Res. 29, 69–79 (2015).
    Google Scholar 
    27.Vargas González, J. D. J. et al. Breeding habitat suitability index for the harpy eagle in Panama: conservation implications. J. Raptor Res. Press, (2020).28.Touchton, J., Hsu, Y. & Palleroni, A. Foraging ecology of reintroduced captive-bred subadult harpy eagles (Harpia harpyja) on Barro Colorado Island, Panama. Ornitol. Neotrop. 13, 365–379 (2002).
    Google Scholar 
    29.Miranda, E. B. P., Peres, C. A., Marini, M. Â. & Downs, C. T. Harpy Eagle (Harpia harpyja) nest tree selection: logging in Amazonian forests threatens Earth’s largest eagle. Biol. Conserv. 250, 108754 (2020).
    Google Scholar 
    30.Muñiz-López, R. et al. Movements of Harpy Eagles Harpia harpyja during their first two years after hatching Movements of Harpy Eagles Harpia harpyja during their first two years after hatching. Bird Study 3657, 509–514 (2016).
    Google Scholar 
    31.Muñiz-López, R. Harpy Eagle (Harpia harpyja) mortality in Ecuador. Stud. Neotrop. Fauna Environ. 30, 1–5 (2017).
    Google Scholar 
    32.Urios, V., Muñiz-López, R. & Vidal-Mateo, J. Juvenile Dispersal of Harpy Eagles (Harpia harpyja) in Ecuador. J. Raptor Res. 51, 439–445 (2017).
    Google Scholar 
    33.Monsalvo, J. A. B., Heming, N. M. & Marini, M. Â. Breeding biology of neotropical accipitriformes: current knowledge and research priorities. Rev. Bras. Ornitol. 26, 151–186 (2018).
    Google Scholar 
    34.Hall, C. Harpy Eagle Studbook Harpia harpyja North American Regional. (2011).35.Alvarez-Cordero, E. Biology and conservation of the harpy eagle in Venezuela and Panama. DSc Thesis. (University of Florida, Florida, USA, 1996).36.Rettig, N. Breeding behavior of the harpy eagle (Harpia harpyja). Auk 95, 629–643 (1978).
    Google Scholar 
    37.Giudice, R., Piana, R. & Williams, M. Tree architecture as a determinant factor in nest-tree selection by Harpy Eagles. In Neotropical Raptors (eds. Bildstein, K. L., Barber, D. R. & Zimmerman, A.) 14–22 (Hawk Mountain Sanctuary, 2007).38.Miranda, E. B. P. de, Peres, C. A. & Downs, C. T. Perceptions of livestock predation (or the lack of it) drive the persecution of Earth’s largest eagle. Anim. Conserv. Press (2020).39.Giraldo-Amaya, M. A. T. E. O., Aguiar-Silva, F. H., Aparício, K. M. & Zuluaga, S. Human persecution on the harpy eagle: a widespread threat?. J. Raptor Res. 55, 1–6 (2020).
    Google Scholar 
    40.Terborgh, J. et al. Ecological meltdown in predator-free forest fragments. Science (80-). 294, 1923–1926 (2001).ADS 
    CAS 

    Google Scholar 
    41.Aguiar-Silva, H. Uso e seleção de recursos por harpia em múltiplas escalas espaciais: persistência e vulnerabilidade (INPA, 2016).42.Aguiar-Silva, F., Sanaiotti, T. & Luz, B. Food habits of the Harpy Eagle, a top predator from the Amazonian rainforest canopy. J. Raptor Res. 48, 24–45 (2014).
    Google Scholar 
    43.Silva, D. A. Comunidade de mamíferos de médio e grande porte em fragmentos florestais da amazônia meridional (Unemat – Nova Xavantina, 2016).44.Miranda, E. B. P., Campbell-Thompson, E., Muela, A. & Vargas, F. H. Sex and breeding status affect prey composition of Harpy Eagles Harpia harpyja. J. Ornithol. 159, 141–150 (2017).
    Google Scholar 
    45.Terborgh, J. Five New World Primates: A Study in Comparative Ecology (Princeton University Press, 2014).46.Oliveira, A. T. M. et al. Primate and ungulate responses to teak agroforestry in a southern Amazonian landscape. Mamm. Biol. 96, 45–52 (2019).
    Google Scholar 
    47.Michalski, F. & Peres, C. A. Gamebird responses to anthropogenic forest fragmentation and degradation in a southern Amazonian landscape. PeerJ 5, e3442 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    48.Barbosa, H. Estrutura de comunidades de mamíferos de médio e grande porte em fragmentos florestais da Amazônia Meridional (Unemat – Cáceres, 2012).49.Michalski, F. & Peres, C. A. Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biol. Conserv. 124, 383–396 (2005).
    Google Scholar 
    50.Trinca, C. T. & Ferrari, S. F. Caça em assentamento rural na amazônia matogrossense. Diálogos em ambiente e sociedade no Brasil (2006).51.Schneider, M. & Peres, C. A. Environmental costs of government-sponsored agrarian settlements in Brazilian Amazonia. PLoS ONE 10, e0134016 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    52.Cavalcante, T. et al. Niche overlap between two sympatric frugivorous Neotropical primates: improving ecological niche models using closely-related taxa. Biodivers. Conserv. 29, 2749–2763 (2020).
    Google Scholar 
    53.Peres, C. A. Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conserv. Biol. 15, 1490–1505 (2001).
    Google Scholar 
    54.Bowler, M. et al. Harpy eagles (Harpia harpyja) nesting at Refugio Amazonas, Tambopata, Peru feed on abundant disturbance-tolerant species. Food Webs 24, e00154 (2020).
    Google Scholar 
    55.Cavalcante, T., Tuyama, C. A. & Mourthe, I. Insights into the development of a juvenile harpy eagle’s hunting skills. Acta Amaz 49, 114–117 (2019).
    Google Scholar 
    56.Campbell-Thompson, E., Vargas, F. H., Watson, R. T., Muela, A. & Cáceres, N. C. Effect of sex and age at release on the independence of hacked harpy eagles. J. Raptor Res. 46, 158–167 (2012).
    Google Scholar 
    57.Watson, R. T., McClure, C. J. W., Vargas, F. H. & Jenny, J. P. Trial restoration of the harpy eagle, a large, long-lived, tropical forest raptor panama and belize. J. Raptor Res. 50, 3–22 (2016).
    Google Scholar 
    58.Touchton, J. The Harpy Eagle. In The eagle watchers: Observing and conserving raptors around the world (eds. Tingay, R. & Katzner, T.) 264 (Cornell University Press, 2010).59.Crisostomo, A. C., Alencar, A., Mesquita, I., Silva, I. & Dourado, M. Terras Indígenas Na Amazônia Brasileira: reservas de carbono e barreiras ao desmatamento (2015).60.Villas Boas, O. & Villas Boas, C. A marcha para o oeste: a epopéia da expedição Roncador-Xingu (Globo, 1994).61.Tufiño, P. Cunsi Pindo: The Mistress of the Monkeys (Simbioe, 2007).62.Reina, R. E. & Kensinger, K. M. The Gift of Birds: Featherworking of Native South American Peoples. (University Museum of Archaeology & Anthropology, 1991).63.Anonymous. Lei de Proteção à Fauna, Lei 5.197, de 03 de janeiro de 1967. (1967).64.Campos-Silva, J. V. & Peres, C. A. Community-based management induces rapid recovery of a high-value tropical freshwater fishery. Sci. Rep. 6, 34745 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    65.Antunes, A. P. et al. Subsistence hunting rights in the Brazilian Amazon. Land Use Policy 84, 1–11 (2019).
    Google Scholar 
    66.Aleixo, A. & Galetti, M. The conservation of the avifauna in a lowland Atlantic forest in south-east Brazil. Bird Conserv. Int. 7, 235–261 (1997).
    Google Scholar 
    67.Lees, A. C. & Peres, C. A. Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conserv. Biol. 22, 439–449 (2008).PubMed 

    Google Scholar 
    68.Zimbres, B., Machado, R. B. & Peres, C. A. Anthropogenic drivers of headwater and riparian forest loss and degradation in a highly fragmented southern Amazonian landscape. Land Use Policy 72, 354–363 (2018).
    Google Scholar 
    69.Michalski, F., Metzger, J. P. & Peres, C. A. Rural property size drives patterns of upland and riparian forest retention in a tropical deforestation frontier. Glob. Environ. Change 20, 705–712 (2010).
    Google Scholar 
    70.Mori, S. A. & Prance, G. T. Taxonomy, ecology, and economic botany of the Brazil nut (Bertholletia excelsa Humb. & Bonpl.: Lecythidaceae). Adv. Econ. Bot. 8, 130–150 (1990).
    Google Scholar 
    71.Buckley, R. Conservation Tourism (CAB International, 2010).72.Ribeiro, S. M. C. et al. Can multifunctional livelihoods including recreational ecosystem services (RES) and non timber forest products (NTFP) maintain biodiverse forests in the Brazilian Amazon?. Ecosyst. Serv. 31, 517–526 (2018).
    Google Scholar 
    73.Strand, J. et al. Spatially explicit valuation of the Brazilian Amazon Forest’s Ecosystem Services. Nat. Sustain. 1, 657 (2018).
    Google Scholar 
    74.Kirkby, C. A. et al. Closing the ecotourism-conservation loop in the Peruvian Amazon. Environ. Conserv. 38, 6–17 (2011).
    Google Scholar 
    75.Kirkby, C. A. et al. The market triumph of ecotourism: an economic investigation of the private and social benefits of competing land uses in the Peruvian Amazon. PLoS ONE 5, e13015 (2010).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Vianna, G. M. et al. Shark-diving tourism as a financing mechanism for shark conservation strategies in Malaysia. Mar. Policy 94, 220–226 (2018).
    Google Scholar 
    77.Fearnside, P. M. Deforestation in Brazilian Amazonia: history, rates, and consequences. Conserv. Biol. 19, 680–688 (2005).
    Google Scholar 
    78.Junior, C. S. & Lima, M. Soy Moratorium in Mato Grosso: deforestation undermines the agreement. Land Use Policy 71, 540–542 (2018).
    Google Scholar 
    79.Lima, M. et al. The paradoxical situation of the white-lipped peccary (Tayassu pecari) in the state of Mato Grosso, Brazil. Perspect. Ecol. Conserv. 17, 36–39 (2019).
    Google Scholar 
    80.Eri, M. et al. Capitalizing on opportunities provided by pasture sudden death to enhance livestock sustainable management in Brazilian Amazonia. Environ. Dev. 4, 100499 (2020).
    Google Scholar 
    81.Anonymous. Novo Código Florestal, Lei 12.651 de 25 de maio de 2012, Dispõe sobre a proteção da vegetação nativa (Subchefia de assuntos jurídicos, 2012).82.Zimbres, B., Peres, C. A. & Machado, R. B. Terrestrial mammal responses to habitat structure and quality of remnant riparian forests in an Amazonian cattle-ranching landscape. Biol. Conserv. 206, 283–292 (2017).
    Google Scholar 
    83.Koeppen, W. Climatologia: con un estudio de los climas de la tierra (1948).84.Radam-Brasil. Projeto Radam-Brasil: levantamento de recursos naturais (1983).85.Ayres, J. M. Observações sobre a ecologia e o comportamento dos cuxiús (Chiropotes albinasus e Chiropotes satanas, Cebidae: Primates) (1981).86.Miranda, E. B. P. de et al. Harpy Eagle nest activity patterns: Potential ecotourism and conservation opportunities in the Amazon Forest. Bird Conserv. Int. (in press) (2021).87.Rosenfield, R. N., Grier, J. W. & Fyfe, R. W. reducing management and research disturbance. In Raptor Research and Management Techniques (ed. Bird, D. M.) 351–364 (Hancock House Publishers, 2007).88.Pagel, J. E. & Thorstrom, R. K. Accessing nests. In Raptor Research and Management Techniques (ed. Bird, D. M.) 171–180 (Hancock House Publishers, 2007).89.Ellis, D. H. & Schimitt, N. J. Behavior of the Golden Eagle: An Illustrated Ethogram. (Hancock House Publishers, 2017).90.Ferguson-Lees, J. & Christie, D. Raptors of the World (Houghton Mifflin Harcourt, 2001).91.Brown, D. A test of randomness of nest spacing. Wildfowl 26, 102–103 (1975).
    Google Scholar 
    92.Emmons, L. & Feer, F. Neotropical Rainforest Mammals: A Field Guide (University of Chicago Press, 1997).93.Sick, H. Ornitologia brasileira, uma introdução (Universidade de Brasília, 1984).94.Goffart, M. Function and Form in the Sloth (Pergamon Press, 1971).95.Dunning, J. Handbook of Avian Body Masses (CRC, 1993).
    Google Scholar 
    96.Gotelli, N. & Aaron, M. A Primer of Ecological Statistics (Sinauer Associates, 2005).97.Krebs, C. Ecological Methodology (Benjamin/Cummings, 1999).98.Ashe, E., Noren, D. P. & Williams, R. Animal behaviour and marine protected areas: incorporating behavioural data into the selection of marine protected areas for an endangered killer whale population. Anim. Conserv. 13, 196–203 (2010).
    Google Scholar 
    99.Miranda, E. B. P., Peres, C. A. & Downs, C. T. Changes in soil fertility mosaics in the Amazon Forest induced by an apex predator. Press (2020).100.R Core. R: A Language and Environment for Statistical Computing. (2020). More