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

    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

  • in

    Quantifying finer-scale behaviours using self-organising maps (SOMs) to link accelerometery signatures with behavioural patterns in free-roaming terrestrial animals

    Data collectionData were collected in the Sunshine Coast region in Queensland, Australia (− 26.65° S, 153.07° E), from February to April 2019. All methods were carried out in accordance with relevant guidelines and regulations. All experimental protocols and methods were approved and carried out in compliance with the ARRIVE guidelines under the approval of the University of the Sunshine Coast (USC) Animal Ethics permit (ANA/16/109T); Human Ethics permit (A181114) and in conjunction with the Sunshine Coast Council (SCC) Local Law permit (OM18/19).
    Animals used in the trialsWe recruited 10 domestic cats through an approved media release (males n = 6; females n = 4; weight 2.8–8.4 kg; age 1.5–12 years; body length 38–53 cm; foreleg length 16–19 cm). As per the Sunshine Coast Council local law requirements, all cats had to be neutered, registered and microchipped to participate in the study.
    EquipmentWe fitted each cat with a retail harness, to which we attached a tri-axial accelerometer (AX3; Axivity, Newcastle University, UK; 23 × 32.5 × 8.9 mm; 11 g) using cable ties (Fig. 1a). The accelerometer was initialised using the Open Movement Graphical User Interaction application (OMGUI; V1.0.0.37). Because a trade-off exists between data resolution and battery life, we logged data at 50 Hz and with a dynamic range of ± 8 g, with a 13-bit resolution, similar to a previous study23. When combined with the in-built memory storage capacity of 512 MB, and battery limitations, this configuration resulted in a maximum of 8–14 days of data collection. The quartz Real Time Clock and calendar provided a timestamp with a frequency of 32.768 kHz and a precision of ± 50 ppm, with manufacturer specifications indicating a drift of 0.18 s per hour. To overcome this drift over the eight days, we calibrated devices by video recording the signals of five claps/taps on the device, at the start and end of each individual data collection period, and also at random times during the day.Figure 1(a) The anatomical position of the accelerometer (AX3) on the sternum of the cat. (b) The activity of swatting stimulated by the use of a feather. (c) The axis orientation of the accelerometer planes, which are represented in the accelerometer trace data in the MATLAB interface. Fore-aft (surge), lateral (sway) and dorso-ventral (heave) movement is reflected in the X, Y and Z signals.Full size imageWe positioned the accelerometer on the scapular brace-strap of the harness, inverted such that the accelerometer was on the sternum of the cat (Fig. 1a–c). Field trials over four months on four cats in the study determined that this position, in comparison with mounting on the dorsal cranial median plane, did not interfere with the animals’ balance; it also removed all of the abnormal movement behaviours and unnecessary discomfort to the cat2. The positioning of the logging device on the frontal anterior, median plane, resulted in the primary axis for fore-aft (surge), lateral (sway) and dorso-ventral (heave) movement to be reflected in the X, Y and Z signals, respectively (Fig. 1c).The accelerometer harness was used in conjunction with the CatBib for the relevant treatment periods. The total combined mass of the harness, accelerometer and Catbib was to 34.1 g, with a minimum cat mass of 2.8 kg, suggesting the equipment did not weigh above 1.2% of total body weight in any cat studied. The CatBib is a prey protector device, manufactured from a lightweight, washable neoprene material, that is attached to a cat’s safety collar (Fig. 1b). The dimensions of the bib are 17.5 mm × 17.5 mm × 6.5 mm, with a total mass of 23.1 g and it is purple in colour. All cats adjusted to the harness and CatBib within the first hour of deployment and no subsequent adjustments were required. All cats had unrestricted access to roam freely outside during the eight days of field trials.To capture training data, each cat was filmed with a GoPro + 3 Hero device (H.264—1920 × 1080; f/2.8; 60 fps), undertaking natural or stimulated active behaviours through play (Fig. 1b). These activities or behaviours were manually documented to track the activity, date and the timestamps. We conducted two treatments over the eight days: in the first, cats were fitted with CatBib, whereas in the other, bibs were not worn. Each treatment was conducted for four consecutive days, and the sequence of treatments for each cat was randomised. The accelerometer device on the harness was left on the cats for the entire field trial and recorded continuously for the eight days (~ 192 h per cat; total = 2304 h).Data analysisEach accelerometer trace file was exported as a raw binary file through OMIGUI and imported into a custom-built MATLAB GUI. To build our training dataset, the video file timestamp information, determined using Mediainfo (version 18.08, 2018), was used to define the start time for a subset of the accelerometer trace, and the video length to define the end point (Supp. Fig. 1). Offsets between the accelerometer trace and video files were determined using the closest calibrated tap signal trace for each day. We were able to watch each video file in synchrony with the accelerometer trace, and manually annotate each movement/activity from the video files to the accelerometer subset (Clemente et al.)24 (Supp. 1.1. Matlab interface instructions; Supp. Fig. 1).We grouped activities according to behaviour into three classes: Sedentary, Eating and Locomotive and Hunting. We further subdivided each group into behaviours. Sedentary included lying, sitting, grooming and watching; Eating and Locomotive included—eating/drinking, walking, trotting; and for Hunting—galloping, jumping, pouncing, swatting, biting/holding (Supp. Table 1).The accelerometer trace was then further divided into rolling epochs of 50 samples in length, using 1 s duration at 50 Hz to ensure intensive acceleratory bursts of short duration such as jumping and pouncing are captured. The behaviour with the maximum frequency within each epoch was assigned as that epoch’s label. Raw accelerometer data in each epoch was assigned as that epoch’s label. Raw accelerometer data in each epoch was summarized using 26 of the most effective variables for procedure accuracy identified by Tatler et al.25. We included: axial acceleration (X, Y, Z),mean acceleration (X, Y, Z); minimum acceleration.(X, Y, Z); maximum acceleration (X, Y, Z); standard deviation of acceleration (X, Y, Z); Signal Magnitude Area, minimum Overall Dynamic Body Acceleration (ODBA); maximum ODBA, minimum Vectorial Dynamic Body Acceleration VDBA; maximum VDBA, sum ODBA; sum VDBA; correlation (XY, YZ, XZ); skewness (X, Y, Z); and kurtosis (X, Y, Z)25 (See Supp. Table 2 for a detailed description of each variable). Finally, we coded the two treatments: BibON and BibOFF and included this information in the training data set.Classification modellingTo determine whether we could predict cat hunting behaviours, we analysed the training data sets using a Kohonen super Self Organising Map (SOM) in the R package ‘Kohonen’ version 2.0.1926,27.Machine learning procedures such as random forest and support vector machines each provide computationally powerful methods of data classification, however each method is not equal in how it visualises its output. SOMS have been used in behavioural studies10,13,14,15 for their ability to efficiently create easily interpreted maps and identify patterns of behaviour. Self-organizing maps differ from other artificial neural networks as they apply competitive learning as opposed to error-correction learning. In this study, a self-organising map algorithm was chosen for its efficiency in visualising multi-dimensional and complex data onto an easily interpreted two dimensional map output. SOMs also have the ability to visualise which variables are most influential with the use of component planes (Fig. 3b–e) and unlike other procedures mentioned, SOMs use cluster analysis which in this study aids in identifying similar behaviours and visualising them closer together (in clusters) on the map output.To prepare data for the SOM function a random sample of the classifiers for the trained data were extracted, along with their associated behaviour, and combined into a list with 2 elements (measurements and activity). This list was then input into the function supersom.R function, with the grid argument defined using the somgrid.R function [e.g. supersom(TrainingData, grid = somgrid(7, 7, “hexagonal”))]. The 7 × 7 grid function was chosen based on a sensitivity analysis exploring all combinations of grids between 4 to 9 units in length (n = 36, Supp. Fig. 2). The 7 × 7 grid represented the grid which produced the highest accuracy and map symmetry26,28,29. We further tested the effect of the number of times the complete data set is presented to the network by varying the rlen argument in the supersom.R function. We found no obvious increase in overall accuracy with increased iterations, and therefore used the default length of 100 times (Supp. Figure 3). Each supersom procedure created was then tested using the predict.R function, with the newdata argument directed to a testing data set, which was a similar 2 element list containing all samples not included in the training data set. The result of this test was then assembled into a confusion matrix using the table.R function with predictions compared with the known behaviours in the test data set [e.g. table(predictions = ssom.pred$predictions$activity, activity = testData$activity) ]. A confusion matrix is a table where each row represents the instances in a predicted class, while each column represents the instances in the observed class, allowing mislabelled epochs to be easily identified. The confusion matrix was then finally used to compute four specific accuracy metrics—sensitivity (or recall), precision, specificity, as well as overall accuracy.To identify relationships between the size of training dataset, we trained a randomised subset of the BibOFF training data, to predict the remaining BibOFF data from all cats. We tested 35 different subset sample sizes from 100 to 100,000, replicating each sample size ten times (with replacement) to determine variation at each sample size.We then tested the extent to which accelerometer traces are modified by the presence of the CatBib. This modification was indicated by a change in overall prediction accuracy of the SOM between BibOFF and BibON treatments. To do this, we trained the SOM using a subset of the trained data for BibOFF and tested it against annotated classified BibON samples. In order to statistically compare results from bootstrap resampling, we took the median among bootstrap samples as the estimate of performance and quantified uncertainty using the corresponding 2.5th and 97.5th percentiles to represent credible 95% confidence intervals (CIs). We chose the median as a measure of central tendency, because resampling distributions were truncated at 1, so were skewed. If CIs for any pair of estimates (medians) do not overlap, then this is evidence of a significant difference between the estimates. If, however, one estimated median fell within the confidence interval for another estimate, then this was used as evidence of a lack of significant difference. For all other outcomes, differences are equivocal, and we interpreted them tentatively on the basis of the relative overlap in CIs.Finally we compared the output of the SOM with the output from a decision tree classification method using a random forest (RF) approach from the randomForest.R package30. We chose random forest as a comparison as this method has previously been shown to perform better than other similar methods (e.g. k-nearest neighbour, support vector machine, and naïve Bayes) when classifying behavioural data on free moving animals25,31. We trained both the SOM and RF procedures using the same 20,000 randomly selected epochs, and compared the overall accuracy for predicting the behaviour for the remaining ~ 192,000 epochs. The SOM was built using a 7 × 7 grid patterns, with the rlen argument set to 100. The RF was built with the number of trees set to 100 and the number of variables randomly sampled as candidates at each split set to 4. More

  • in

    Water quality drives the regional patterns of an algal metacommunity in interconnected lakes

    1.Leibold, M. A. et al. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7, 601–613. https://doi.org/10.1111/j.1461-0248.2004.00608.x (2004).Article 

    Google Scholar 
    2.McGill, B. J., Enquist, B. J., Weiher, E. & Westoby, M. Rebuilding community ecology from functional traits. Trends Ecol. Evol. 21, 178–185. https://doi.org/10.1016/j.tree.2006.02.002 (2006).Article 
    PubMed 

    Google Scholar 
    3.Kraft, N. et al. Community assembly, coexistence, and the environmental filtering metaphor. Funct. Ecol. https://doi.org/10.1111/1365-2435.12345 (2014).Article 

    Google Scholar 
    4.de la Sancha, N. U., Higgins, C. L., Presley, S. J. & Strauss, R. E. Metacommunity structure in a highly fragmented forest: has deforestation in the Atlantic Forest altered historic biogeographic patterns?. Divers. Distrib. 20, 1058–1070. https://doi.org/10.1111/ddi.12210 (2014).Article 

    Google Scholar 
    5.Leibold, M. & Mikkelson, G. Coherence, species turnover, and boundary clumping: Elements of meta-community structure. Oikos 97, 237–250. https://doi.org/10.1034/j.1600-0706.2002.970210.x (2002).Article 

    Google Scholar 
    6.Presley, S., Higgins, C. & Willig, M. A comprehensive framework for the evaluation of metacommunity structure. Oikos 119, 908–917. https://doi.org/10.1111/j.1600-0706.2010.18544.x (2010).Article 

    Google Scholar 
    7.Dallas, T. & Drake, J. M. Relative importance of environmental, geographic, and spatial variables on zooplankton metacommunities. Ecosphere 5, 1–13. https://doi.org/10.1890/ES14-00071.1 (2014).Article 

    Google Scholar 
    8.Heino, J., Mykrä, H. & Muotka, T. Temporal variability of nestedness and idiosyncratic species in stream insect assemblages. Divers. Distrib. 15, 198–206. https://doi.org/10.1111/j.1472-4642.2008.00513.x (2009).Article 

    Google Scholar 
    9.Henriques-Silva, R., Lindo, Z. & Peres-Neto, P. R. A community of metacommunities: exploring patterns in species distributions across large geographical areas. Ecology 94, 627–639. https://doi.org/10.1890/12-0683.1 (2013).Article 
    PubMed 

    Google Scholar 
    10.Dallas, T. & Drake, J. M. Relative importance of environmental, geographic, and spatial variables on zooplankton metacommunities. Ecosphere 5, art104. https://doi.org/10.1890/ES14-00071.1 (2014).Article 

    Google Scholar 
    11.Erős, T. et al. Quantifying temporal variability in the metacommunity structure of stream fishes: The influence of non-native species and environmental drivers. Hydrobiologia 722, 31–43. https://doi.org/10.1007/s10750-013-1673-8 (2014).Article 

    Google Scholar 
    12.Fernandes, I. M., Henriques-Silva, R., Penha, J., Zuanon, J. & Peres-Neto, P. R. Spatiotemporal dynamics in a seasonal metacommunity structure is predictable: The case of floodplain-fish communities. Ecography 37, 464–475. https://doi.org/10.1111/j.1600-0587.2013.00527.x (2014).Article 

    Google Scholar 
    13.Tonkin, J. D. et al. The role of dispersal in river network metacommunities: Patterns, processes, and pathways. Freshw. Biol. 63, 141–163. https://doi.org/10.1111/fwb.13037 (2018).Article 

    Google Scholar 
    14.Kim, S., Chung, S., Park, H., Cho, Y. & Lee, H. Analysis of environmental factors associated with cyanobacterial dominance after river weir installation. Water https://doi.org/10.3390/w11061163 (2019).Article 

    Google Scholar 
    15.Deng, J. et al. Effects of nutrients, temperature and their interactions on spring phytoplankton community succession in Lake Taihu, China. PLoS ONE 9, e113960–e113960. https://doi.org/10.1371/journal.pone.0113960 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Yang, J., Jiang, H., Liu, W. & Wang, B. Benthic algal community structures and their response to geographic distance and environmental variables in the Qinghai-Tibetan lakes with different salinity. Front. Microbiol. 9, 578–578. https://doi.org/10.3389/fmicb.2018.00578 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    17.Zhou, J. et al. Microbial community structure and associations during a marine dinoflagellate bloom. Front. Microbiol. 9, 1201. https://doi.org/10.3389/fmicb.2018.01201 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.RDevelopmentCoreTeam. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).
    Google Scholar 
    19.Baird, R. B. Standard Methods for the Examination of Water and Wastewater 23rd edn. (Water Environment Federation, American Public Health Association, 2017).
    Google Scholar 
    20.Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
    Google Scholar 
    21.Cajo, J. F. T. B. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67, 1167–1179. https://doi.org/10.2307/1938672 (1986).Article 

    Google Scholar 
    22.Tuomisto, H. A diversity of beta diversities: straightening up a concept gone awry. Part 2. Quantifying beta diversity and related phenomena. Ecography 33, 23–45. https://doi.org/10.1111/j.1600-0587.2009.06148.x (2010).Article 

    Google Scholar 
    23.Clements, F. E. Nature and structure of the climax. J. Ecol. 24, 252–284. https://doi.org/10.2307/2256278 (1936).Article 

    Google Scholar 
    24.Kurthen, A. L. et al. Metacommunity structures of macroinvertebrates and diatoms in high mountain streams, Yunnan, China. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2020.571887 (2020).Article 

    Google Scholar 
    25.Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R. & Cushing, C. E. The river continuum concept. Can. J. Fish. Aquat. Sci. 37, 130–137. https://doi.org/10.1139/f80-017 (1980).Article 

    Google Scholar 
    26.López-González, C., Presley, S. J., Lozano, A., Stevens, R. D. & Higgins, C. L. Metacommunity analysis of Mexican bats: environmentally mediated structure in an area of high geographic and environmental complexity. J. Biogeogr. 39, 177–192. https://doi.org/10.1111/j.1365-2699.2011.02590.x (2012).Article 

    Google Scholar 
    27.Heino, J., Soininen, J., Alahuhta, J., Lappalainen, J. & Virtanen, R. Metacommunity ecology meets biogeography: effects of geographical region, spatial dynamics and environmental filtering on community structure in aquatic organisms. Oecologia 183, 121–137. https://doi.org/10.1007/s00442-016-3750-y (2017).ADS 
    Article 
    PubMed 

    Google Scholar 
    28.Heino, J. & Alahuhta, J. Elements of regional beetle faunas: faunal variation and compositional breakpoints along climate, land cover and geographical gradients. J. Anim. Ecol. 84, 427–441. https://doi.org/10.1111/1365-2656.12287 (2015).Article 
    PubMed 

    Google Scholar 
    29.Mallin, M. A., McIver, M. R., Ensign, S. H. & Cahoon, L. B. Photosynthetic and heterotrophic impacts of nutrient loading to blackwater streams. Ecol. Appl. 14, 823–838. https://doi.org/10.1890/02-5217 (2004).Article 

    Google Scholar 
    30.B-Béres, V. et al. Autumn drought drives functional diversity of benthic diatom assemblages of continental intermittent streams. Adv. Water Resour. 126, 129–136. https://doi.org/10.1016/j.advwatres.2019.02.010 (2019).ADS 
    Article 

    Google Scholar 
    31.Kagalou, I., Petridis, D. & Tsimarakis, G. Seasonal variation of water quality parameters and plankton in a shallow Greek lake. J. Freshw. Ecol. 18, 199–206. https://doi.org/10.1080/02705060.2003.9664485 (2003).CAS 
    Article 

    Google Scholar 
    32.Padisák, J., Crossetti, L. O. & Naselli-Flores, L. Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621, 1–19. https://doi.org/10.1007/s10750-008-9645-0 (2009).Article 

    Google Scholar 
    33.Schabhüttl, S. et al. Temperature and species richness effects in phytoplankton communities. Oecologia 171, 527–536. https://doi.org/10.1007/s00442-012-2419-4 (2013).ADS 
    Article 
    PubMed 

    Google Scholar 
    34.Chen, S. et al. Geographical patterns of algal communities associated with different urban lakes in China. Int. J. Environ. Res. Public Health 17, 1009. https://doi.org/10.3390/ijerph17031009 (2020).Article 
    PubMed Central 

    Google Scholar 
    35.Hwang, S.-J., Kim, H.-S., Shin, J.-K., Oh, J.-M. & Kong, D.-S. Grazing effects of a freshwater bivalve (Corbicula leana Prime) and large zooplankton on phytoplankton communities in two Korean lakes. Hydrobiologia 515, 161–179. https://doi.org/10.1023/B:HYDR.0000027327.06471.1e (2004).Article 

    Google Scholar 
    36.Moss, B. et al. How important is climate? Effects of warming, nutrient addition and fish on phytoplankton in shallow lake microcosms. J. Appl. Ecol. 40, 782–792. https://doi.org/10.1046/j.1365-2664.2003.00839.x (2003).Article 

    Google Scholar 
    37.Chen, S. et al. Local habitat heterogeneity determines the differences in benthic diatom metacommunities between different urban river types. Sci. Total Environ. 669, 711–720. https://doi.org/10.1016/j.scitotenv.2019.03.030 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar  More

  • in

    Spatio-temporal distribution patterns of Plutella xylostella (Lepidoptera: Plutellidae) in a fine-scale agricultural landscape based on geostatistical analysis

    1.Zalucki, M. P. et al. Estimating the economic cost of one of the world’s major insect pests, Plutella xylostella: Just how long is a piece of string?. J. Econ. Entomol. 105, 1115–1129 (2012).PubMed 
    Article 

    Google Scholar 
    2.Li, Z. Y., Feng, X., Liu, S. S., You, M. S. & Furlong, M. J. Biology, ecology, and management of the diamondback moth in China. Annu. Rev. Entomol. 61(1), 277–296 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Talekar, N. S. & Shelton, A. M. Biology, ecology, and management of the diamondback moth. Annu. Rev. Entomol. 38(1), 275–301 (1993).Article 

    Google Scholar 
    4.Zhu, L. et al. Population dynamics of diamondback moth, Plutella xylostella (L.) in northern China: The effect of migration, cropping patterns and climate. Pest Manag. Sci. 74(8), 1845–1853 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Furlong, M. J., Wright, D. J. & Dosdall, L. M. Diamondback moth ecology and management: Problems, progress, and prospects. Annu. Rev. Entomol. 58, 517–541 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Sayyed, A. H., Saeed, S., Noorulane, M. & Crickmore, N. Genetic, biochemical, and physiological characterization of spinosad resistance in Plutella xylostella (Lepidoptera: Plutellidae). J. Econ. Entomol. 101(5), 1658–1666 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Machekano, H., Mvumi, B. M. & Nyamukondiwa, C. Loss of coevolved basal and plastic responses to temperature may underlie trophic level host-parasitoid interactions under global change. Biol. Control 118, 44–54 (2018).Article 

    Google Scholar 
    8.Chapman, J. W. et al. High-altitude migration of the diamondback moth Plutella xylostella to the U.K.: A study using radar, aerial netting, and ground trapping. Ecol. Entomol. 27(6), 641–650 (2002).Article 

    Google Scholar 
    9.Mazzi, D. & Dorn, S. Movement of insect pests in agricultural landscapes. Ann. Appl. Biol. 160(2), 97–113 (2012).Article 

    Google Scholar 
    10.Wei, S. J. et al. Genetic structure and demographic history reveal migration of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) from the southern to Northern Regions of China. PLoS ONE 8(4), e59654 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Fu, X., Xing, Z., Liu, Z., Ali, A. & Wu, K. Migration of diamondback moth, Plutella xylostella, across the Bohai Sea in northern China. Crop Prot. 64, 143–149 (2014).Article 

    Google Scholar 
    12.Li, Z. et al. Population dynamics and management of diamondback moth (Plutella xylostella) in China: The relative contributions of climate, natural enemies and cropping patterns. Bull. Entomol. Res. 106(2), 197–214 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Machekano, H. et al. Disentangling factors limiting diamondback moth, Plutella xylostella (L.), spatio-temporal population abundance: A tool for pest forecasting. J. Appl. Entomol. 143, 670–682 (2019).CAS 
    Article 

    Google Scholar 
    14.Eziah, V. Y., Rose, H. A., Wilkes, M., Clift, A. D. & Mansfiled, S. Population dynamics of the diamondback moth Plutella xylostella L. (Lepidoptera: Yponomeutidae) in the Sydney region of Australia. Int. J. Biol. Chem. Sci. 4(4), 1062–1082 (2011).
    Google Scholar 
    15.Alam, T., Raju, S. V. S., Raghuraman, M. & Kumar, K. R. Population dynamics of diamondback moth, Plutella xylostella (L.) on cauliflower Brassica oleracea L. var. Botrytis in relation to weather factors of eastern uttar pradesh region. J. Exp. Zool. India 19(1), 289–292 (2016).
    Google Scholar 
    16.Karimzadeh, J., Bonsall, M. B. & Wright, D. J. Bottom-up and top-down effects in a tritrophic system: The population dynamics of Plutella xylostella (L.)-Cotesia plutellae (Kurdjumov) on different host plants. Ecol. Entomol. 29(3), 285–293 (2004).Article 

    Google Scholar 
    17.Soufbaf, M., Fathipour, Y., Karimzadeh, J. & Zalucki, M. P. Effects of plant availability on population size and dynamics of an insect community: Diamondback moth and two of its parasitoids. Bull. Entomol. Res. 104(4), 418–431 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    18.Li, Z. Y. et al. Population dynamics and ‘outbreaks’ of diamondback moth, Plutella xylostella, in Guangdong province, China: Climate or the failure of management?. J. Econ. Entomol. 105(3), 739–752 (2012).PubMed 
    Article 

    Google Scholar 
    19.Sutcliffe, L. M. E., Batáry, P., Becker, T., Orci, K. M. & Leuschner, C. Both local and landscape factors determine plant and Orthoptera diversity in the semi-natural grasslands of Transylvania, Romania. Biodivers. Conserv. 24(2), 229–245 (2015).Article 

    Google Scholar 
    20.Carrière, Y. et al. Effects of local and landscape factors on population dynamics of a cotton pest. PLoS ONE 7(6), e39862 (2012).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    21.Moroń, D., Skórka, P., Lenda, M., Celary, W. & Tryjanowski, P. Railway lines affect spatial turnover of pollinator communities in an agricultural landscape. Divers. Distrib. 23(9), 1090–1097 (2017).Article 

    Google Scholar 
    22.Skellern, M. P., Welham, S. J., Watts, N. P. & Cook, S. M. Meteorological and landscape influences on pollen beetle immigration into oilseed rape crops. Agric. Ecosyst. Environ. 241, 150–159 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Meisner, M. H., Zaviezo, T. & Rosenheim, J. A. Landscape crop composition effects on cotton yield, Lygus hesperus densities and pesticide use. Pest Manag. Sci. 73(1), 232–239 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Furlong, M. J. et al. Ecology of diamondback moth in Australian canola: Landscape perspectives and the implications for management. Aust. J. Exp. Agric. 48(12), 1494–1505 (2008).Article 

    Google Scholar 
    25.Rogers, C. D., Guimaraes, R. M. L., Evans, K. A. & Rogers, S. A. Spatial and temporal analysis of wheat bulb fly (Delia coarctata, Fallén) oviposition: Consequences for pest population monitoring. J. Pest Sci. 88, 75–86 (2014).Article 

    Google Scholar 
    26.Silva, G. A. et al. Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag. Sci. 67, 913–920 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Rossi, R. E., Mulla, D. J., Journel, A. G. & Franz, E. H. Geostatistical tools for modeling and interpreting ecological spatial dependence. Ecol. Monogr. 62(2), 277–314 (1992).Article 

    Google Scholar 
    28.Leibhold, A. M., Rossi, R. E. & Kemp, W. P. Geostatistics and geographic information systems in applied insect ecology. Annu. Rev. Entomol. 38(1), 303–327 (1993).Article 

    Google Scholar 
    29.Veran, S. et al. Modeling spatiotemporal dynamics of outbreaking species: Influence of environment and migration in a locust. Ecology 96(3), 737–748 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Martins, J. C. et al. Assessing the spatial distribution of Tuta absoluta (lepidoptera: gelechiidae) eggs in open-field tomato cultivation through geostatistical analysis. Pest Manag. Sci. 74(1), 30–36 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Cocco, A., Serra, G., Lentini, A., Deliperi, S. & Delrio, G. Spatial distribution and sequential sampling plans for Tuta absoluta (Lepidoptera: Gelechiidae) in greenhouse tomato crops. Pest Manag. Sci. 71(9), 1311–1323 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Sciarretta, A., Zinni, A., Mazzocchetti, A. & Trematerra, P. Spatial analysis of Lobesia botrana (lepidoptera: tortricidae) male population in a mediterranean agricultural landscape in Central Italy. Environ. Entomol. 37(2), 382 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Sciarretta, A. & Trematerra, P. Spatio-temporal distribution of Ceratitis capitata population in a heterogeneous landscape in Central Italy. J. Appl. Entomol. 135(4), 241–251 (2011).Article 

    Google Scholar 
    34.Fuzhou. https://baike.baidu.com/item/%E7%A6%8F%E5%B7%9E/165311?fr=Aladdin (2021).35.Fujian Meteorological Service Center. http://fj.cma.gov.cn/#qxfw (2021).36.Farias, P. R. S., Roberto, S. R., Lopes, J. R. S. & Perecin, D. Geostatistical characterization of the spatial distribution of Xylella fastidiosa sharpshooter vectors on citrus. Neotrop. Entmol. 33, 13–20 (2002).Article 

    Google Scholar 
    37.Cambardella, C. A. et al. Field-scale variability of soil proprieties in central Iowa soils. Soil Sci. Soc. Am. J. 58, 1240–1248 (1994).Article 

    Google Scholar 
    38.Zhou, C. B., Lin, Z. F., Xie, S. H. & Ji, X. C. Population dynamics of Plutella xylostella and its influence factors in Hainan. Plant Prot 36(5), 124–128 (2010) (in Chinese, English abstract).
    Google Scholar 
    39.Golizadeh, A. L. I., Kamali, K., Fathipour, Y. & Abbasipour, H. Temperature-dependent development of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) on two Brassicaceous host plants. Insect Sci. 14(4), 309–316 (2007).Article 

    Google Scholar 
    40.Bhagat, P., Yadu, Y. K. & Sharma, G. L. Seasonal incidence and effect of abiotic factors on population dynamics of diamondback moth (Plutella xylostella L.) on cabbage (Brassica oleracea var. Capitata L.) crop. J. Enotomol. Zool. Stud. 6(2), 2001–2003 (2018).
    Google Scholar 
    41.Wang, E. G. & Zheng, Y. L. Seasonal abundance of diamondback moth, Plutella xylostella, adult in Linhai, Zhejiang. Chin. Bull. Entomol. 44(2), 271–274 (2007) (in Chinese, English abstract).ADS 

    Google Scholar 
    42.Lin, X. J., Xie, W. L., Liu, J. B. & Zeng, L. Investigation of the occurrence of Plutella xylostella in Guangzhou. Guangdong Agric. Sci. 36(16), 91–97 (2013) (in Chinese, English abstract).
    Google Scholar 
    43.Harcourt, D. G. Major mortality factors in the population dynamics of the diamondback moth, Plutella maculipennis (Curt.) (Lepidoptera: Plutellidae). Mean. Can. Entomol. 32, 55–66 (1963).Article 

    Google Scholar 
    44.Rahman, M. M., Zalucki, M. P. & Furlong, M. J. Diamondback moth egg susceptibility to rainfall: Effects of host plant and oviposition behavior. Entomol. Exp. Appl. https://doi.org/10.1111/eea.12816 (2019).Article 

    Google Scholar 
    45.Kobori, Y. & Amano, H. Effect of rainfall on a population of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Appl. Entomol. Zool. 38(2), 249–253 (2003).Article 

    Google Scholar 
    46.Ayalew, G., Sciarretta, A., Baumgärtner, J., Ogol, C. & Löhr, B. Spatial distribution of diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), at the field and the regional level in Ethiopia. Int. J. Pest Manag. 54(1), 31–38 (2008).Article 

    Google Scholar 
    47.Mo, J., Greg, B., Mike, K. & Rick, R. Local dispersal of the diamondback moth (Plutella xylostella (L.)) (Lepidoptera: Plutellidae). Environ. Entomol. 32(1), 71–79 (2003).Article 

    Google Scholar 
    48.Xiong, L. G. et al. Biological characteristic of overwintering in the diamondback moth, Plutella xylostella. Plant Prot. 36, 90–93 (2010) (in Chinese, English abstract).
    Google Scholar 
    49.Campos, W. G., Schoereder, J. H. & Sperber, C. F. Does the age of the host plant modulate migratory activity of Plutella xylostella?. Entomol. Sci. 7(4), 323–329 (2004).Article 

    Google Scholar 
    50.Zhao, Z. H., Hui, C., He, D. H. & Ge, F. Effects of position within wheat field and adjacent habitats on the density and diversity of cereal aphids and their natural enemies. Biocontrol 58, 765–776 (2013).CAS 
    Article 

    Google Scholar 
    51.Sciarretta, A. & Trematerra, P. Geostatistical tools for the study of insect spatial distribution: Practical implications in the integrated management of orchard and vineyard pests. Plant Prot. Sci. 50(2), 97–110 (2014).Article 

    Google Scholar 
    52.Saeed, R., Sayyed, A. H., Shad, S. A. & Zaka, S. M. Effect of different host plants on the fitness of diamond-back moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop Prot. 29(2), 178–182 (2010).Article 

    Google Scholar 
    53.Chen, L. L. et al. Cover crops enhance natural enemies while help suppressing pests in a tea plantation. Ann.. Entomol. Soc. Am. 112(4), 348–355 (2019).Article 

    Google Scholar  More