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    Detecting the effects of predator-induced stress on the global metabolism of an ungulate prey using fecal metabolomic fingerprinting

    1.Schmitz, O. J., Krivan, V. & Ovadia, O. Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol. Lett. 7, 153–163 (2004).Article 

    Google Scholar 
    2.Creel, S. & Christianson, D. Relationships between direct predation and risk effects. Trends Ecol. Evol. 23(4), 194–201 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Ritchie, E. G. et al. Ecosystem restoration with teeth: what role for predators?. Trends Ecol. Evol. 27(5), 265–271 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Terborgh, J. & Estes, J. A. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature (Island Press, 2010).
    Google Scholar 
    5.Creel, S. & Winnie, J. A. Responses of elk herd size to fine scale spatial and temporal variation in the risk of predation by wolves. Anim. Behav. 69, 1181–1189 (2005).Article 

    Google Scholar 
    6.Fischhoff, I. R., Sundaresan, S. R., Cordingley, J. & Rubenstein, D. I. Habitat use and movements of plains zebra (Equus burchelli) in response to predation danger from lions. Behav. Ecol. 18, 725–729 (2007).Article 

    Google Scholar 
    7.Latombe, G., Fortin, D. & Parrott, L. Spatio-temporal dynamics in the response of woodland caribou and moose to the passage of grey wolves. J. Anim. Ecol. 83, 185–198 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Prugh, L. R. et al. Designing studies of predation risk for improved inference in carnivore-ungulate systems. Biol. Conserv. 232, 194–207 (2019).Article 

    Google Scholar 
    9.Creel, S., Winnie, J. A. & Christianson, D. Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. PNAS 106(30), 12388–12393 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Dulude-de Broin, F., Hamel, S., Mastromonaco, G. F. & Côté, S. D. Predation risk and mountain goat reproduction: evidence for stress-induced breeding suppression in a wild ungulate. Funct. Ecol. 34(5), 1003–1014 (2020).Article 

    Google Scholar 
    11.Moberg, G. P. & Mench, J. A. The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare (CABI Publishing, 2000).
    Google Scholar 
    12.Boonstra, R. The ecology of stress: a marriage of disciplines. Funct. Ecol. 27, 7–10 (2013).Article 

    Google Scholar 
    13.Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166, 869–887 (2011).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Kelley, K. W. Immunological consequences of changing environmental stimuli. In Animal Stress (ed. Moberg, G. P.) 193–223 (American Physiological Society, Bethesda, 1985).15.Mӧstl, E. & Palme, R. Hormones as indicators of stress. Domest. Anim. Endocrinol. 23, 67–74 (2002).Article 

    Google Scholar 
    16.Ursin, H. & Eriksen, H. R. The cognitive activation theory of stress. Psychoneuroendocrinology 29(5), 567–592 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Lovallo, W. R. Individual differences in reactivity to stress. In Stress and Health. Biological and Psychological Interactions (ed. Lovallo, W. R.) 203–225 (Sage, 2016).18.Patchev, V. K. & Patchev, A. V. Experimental models of stress. Dialogues Clin. Neurosci. 8(4), 417–432 (2006).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Mills, J. L. Scientific Principles of Stress (University of the West Indie Press, 2012).
    Google Scholar 
    20.Henry, J. P. Biological basis of the stress response. Integr. Physiol. Behav. Sci. 27, 66–83 (1992).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Wu, Y., Patchev, A. V., Daniel, G., Almeida, O. F. X. & Spengler, D. Early-life stress reduces DNA methylation of the Pomc gene in male mice. Endocrinology 155(5), 1751–1762 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    22.Novais, A., Monteiro, S., Roque, S., Correia-Neves, M. & Sousa, N. How age, sex and genotype shape the stress response. Neurob. Stress 6, 44–56 (2017).Article 

    Google Scholar 
    23.Romero, L. M. & Gormally, B. M. G. How truly conserved is the “well-conserved” vertebrate stress response?. Integr. Comp. Biol. 59(2), 273–281 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Millspaugh, J. J. & Washburn, B. E. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen. Comp. Endocrinol. 138, 189–199 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Romero, L. M. Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19(5), 249–255 (2004).PubMed 
    Article 

    Google Scholar 
    26.Johnstone, C. P., Reina, R. D. & Lill, A. Interpreting indices of physiological stress in free-living vertebrates. J. Comp. Physiol. B 182, 861–879 (2012).PubMed 
    Article 

    Google Scholar 
    27.Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F. & Tillisch, K. Gut microbes and the brain: paradigm shift in neuroscience. J. Neurosci. 34, 15490–15496 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Sharon, G., Sampson, T. R., Geschwind, D. H. & Mazmanian, S. K. The central nervous system and the gut microbiome. Cell 167, 915–932 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Mohajeri, M. H., La Fata, G., Steinert, R. E. & Weber, P. Relationship between the gut microbiome and brain function. Nutr. Rev. 76, 481–496 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E. & Savignac, H. M. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 108(38), 16050–16055 (2011).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Beauclercq, S. et al. A multiplatform metabolomic approach to characterize fecal signatures of negative postnatal events in chicks: a pilot study. J Anim. Sci. Biotechnol. 10, 21 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Jianguo, L., Xueyang, J., Cui, W., Changxin, W. & Xuemei, Q. Altered gut metabolome contributes to depression-like behaviors in rats exposed to chronic unpredictable mild stress. Transl. Psychiatry 9, 1–14 (2019).Article 
    CAS 

    Google Scholar 
    33.Valerio, A., Casadei, L., Giuliani, A. & Valerio, M. Fecal metabolomics as a novel non-invasive method for short-term stress monitoring in beef cattle. J. Proteome Res. 19(2), 845–853 (2020).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Nicholson, J. K. et al. Host-gut microbiota metabolic interactions. Science 336, 1262–1267 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    35.Nicholson, J. K., Connelly, J., Lindon, J. C. & Holmes, E. Metabolomics: a platform for studying drug toxicity and gene function. Nat. Rev. Drug Discov. 1, 153–161 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Lindon, J. C., Nicholson, J. K. & Holmes, E. The Handbook of Metabonomics and Metabolomics (Elsevier, 2007).
    Google Scholar 
    37.Matysik, S., Le Roy, C. I., Liebisch, G. & Claus, S. P. Metabolomics of fecal samples: a practical consideration. Trends Food Sci. Technol. 57, 244–255 (2016).CAS 
    Article 

    Google Scholar 
    38.Nicholson, J. K. & Lindon, J. C. Metabonomics. Nature 455, 1054–1056 (2008).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Viant, M. R. Environmental metabolomics using 1H-NMR spectroscopy. Methods Mol. Biol. 410, 137–150 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    40.Ellis, D. I., Dunn, W. B., Griffin, J. L., Allwood, J. W. & Goodacre, R. Metabolic fingerprinting as a diagnostic tool. Pharmacogenomics 8(9), 1243–1266 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Worley, B. & Powers, R. Multivariate analysis in metabolomics. Curr. Metabolomics 1(1), 92–107 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Rivas-Ubach, A. et al. Ecometabolomics: optimized NMR-based method. Methods Ecol. Evol. 4(5), 464–473 (2013).Article 

    Google Scholar 
    43.Chen, M. X., Wang, S. Y., Kuo, C. H. & Tsai, I. L. Metabolome analysis for investigating host-gut microbiota interactions. JFMA 118(1), S10–S22 (2019).
    Google Scholar 
    44.Emwas, A. H. M. The Strengths and weaknesses of NMR spectroscopy and mass spectrometry with particular focus on metabolomics research. In Metabonomics. Methods in Molecular Biology (ed. Bjerrum, J. T.) 1277, 161–193 (Human Press, 2015).45.Emwas, A. H. M. et al. NMR spectroscopy for metabolomics research. Metabolites 9(7), 123 (2019).CAS 
    PubMed Central 
    Article 

    Google Scholar 
    46.Nicholson, J. K., Connelly, J., Lindon, J. C. & Holmes, E. Metabonomics: a platform for studying drug toxicity and gene function. Nat. Rev. Drug Discov. 1, 153–161 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Wiles, G. J., Allen, H. L. & Hayes, G. E. Wolf Conservation and Management Plan for Washington (Washington Department of Fish and Wildlife, 2011).
    Google Scholar 
    48.Schmitz, O. J. & Trussell, G. C. Multiple stressors, state-dependence and predation risk-foraging trade-offs: toward a modern concept of trait-mediated indirect effects in communities and ecosystems. Curr. Opin. Behav. 12, 6–11 (2016).Article 

    Google Scholar 
    49.Brown, J. A. Mortality of Range Livestock in Wolf-Occupied Areas of Washington. Thesis. Washington State University, Pullman, WA, USA (2015).50.Fieberg, J. & Kochanny, C. O. Quantification of home range overlap: the importance of the utilization distribution. J. Wildl. Manag. 69, 1346–1359 (2005).Article 

    Google Scholar 
    51.Robert, K., Garant, D. & Pelletier, F. Keep in touch: does spatial overlap correlate with contact rate frequency?. J. Wildl. Manag. 76(8), 1670–1675 (2012).Article 

    Google Scholar 
    52.Angel, S. P. et al. Climate change and cattle production: impact and adaptation. J. Vet. Med. Res. 5(4), 1134 (2018).
    Google Scholar 
    53.Brosh, A. et al. Energy cost of cows’ grazing activity: use of the heart rate method and the global positioning system for direct field estimation. J. Anim. Sci. 84, 1951–1967 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Provenza, F. D. Postingestive feed-back as an elemental determinant of food preference and intake in ruminants. J. Range Manag. 48, 2–17 (1995).Article 

    Google Scholar 
    55.Provenza, F. D. Acquired aversions as the basis for varied diets of ruminants foraging on rangelands. J. Anim. Sci. 74, 2010–2020 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Howery, L. D., Provenza, F. D., Ruyle, G. B. & Jordan, N. C. How do animals learn if rangeland plants are toxic or nutritious?. Rangelands 20, 4–9 (1998).
    Google Scholar 
    57.Davitt, B. B. & Nelson, J. R. Methodology for the determination of DAPA in feces of large ruminants. In Proceedings of the Western States and Provinces Elk Workshop (ed. Nelson, R.W.) 133–147 (Edmonton, 1984).58.Church, D. C. Digestive Physiology and Nutrition of Ruminants I (Oxford Press, 1969).
    Google Scholar 
    59.Sato, S. Leadership during actual grazing in a small herd of cattle. Appl. Anim. Ethol. 8, 53–65 (1982).Article 

    Google Scholar 
    60.Frair, J. L. et al. Resolving issues of imprecise and habitat-biased locations in ecological analyses using GPS telemetry data. Philos. Trans. R. Soc. B 365, 2187–2200 (2010).Article 

    Google Scholar 
    61.Deda, O., Gika, H. G., Wilson, I. D. & Theodoridis, G. A. An overview of fecal preparation for global metabolic profiling. J. Pharm. Biomed. 113, 137–150 (2015).CAS 
    Article 

    Google Scholar 
    62.Landakadurai, B. P., Nagato, E. G. & Simpson, M. J. Environmental metabolomics: an emerging approach to study organism responses to environmental stressors. Environ. Rev. 21, 180–205 (2013).Article 
    CAS 

    Google Scholar 
    63.Wiklund, S. et al. Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. Anal. Chem. 80, 115–122 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Wishart, D. S. et al. HMDB: a knowledgebase for the human metabolome. Nucl. Acids Res. 37, D603–D610 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Frair, J. L. et al. Scale of movement by elk (Cervus elaphus) in response to heterogeneity in forage resources and predation risk. Landsc. Ecol. 20, 273–287 (2005).Article 

    Google Scholar 
    66.Valerio, A. Stress-Mediated and Habitat-Mediated Risk Effects of Free-Ranging Cattle in Washington. Dissertation. Washington State University, Pullman, WA (2019).67.Winnie, J. & Creel, S. Sex-specific behavioral responses of elk to spatial and temporal variation in the threat of wolf predation. Anim. Behav. 73, 215–225 (2007).Article 

    Google Scholar 
    68.Bundy, J. G., Davey, M. P. & Viant, M. R. Environmental metabolomics: a critical review and future perspectives. Metabolomics 5, 3–21 (2009).CAS 
    Article 

    Google Scholar  More

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    Vaccinate in biodiversity hotspots to protect people and wildlife from each other

    Rural areas of low-to-middle-income countries host most biodiversity hotspots, where interactions between people and wildlife are frequent. These regions have less access to vaccines than do urban centres (Local Burden of Disease Vaccine Coverage Collaborators Nature 589, 415–419; 2021).Given the broad potential range of hosts for SARS-CoV-2, we suggest that vaccinating often-neglected populations around protected areas will reduce the risk of people infecting wildlife and creating secondary reservoirs of disease, and thence risking potential reinfection of humans with new variants. This should be considered after vaccination of priority groups, such as older people and health workers.Vaccinating people who live near felids, non-human primates, bats and other animals protects wildlife and limits ‘reverse spillovers’. Such events have been documented for various human respiratory viruses, for instance in wild great apes in west Africa (S. Köndgen et al. Curr. Biol. 18, 260–264; 2008).Non-standard actors, such as national park authorities or conservation organizations, could help vaccination to reach remote regions. This is called a One Health approach: it protects the health of people, animals and the environment. More

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    Contaminant organisms recorded on plant product imports to South Africa 1994–2019

    Sample collection and handlingSource of samples to be screenedSouth Africa currently has 72 official points of entry—8 seaports, 10 airports and 54 land border posts10. The DALRRD has border inspectors at most of these points (although staffing levels have varied considerably). DALRRD border inspectors inspect goods and travellers entering the country for plant contaminants. As part of DALRRD’s biosecurity protocol, three types of samples are collected and sent to DALRRD laboratories in Stellenbosch or Pretoria for further investigation (Fig. 1).

    1.

    Intervention samples. If the border inspector finds or suspects a pest or pathogen in a consignment, he/she will take a sample and send it to one of DALRRD’s diagnostic laboratories. A suspicion of contamination is often the result of quarantine organisms being detected on previous consignments of the same commodity. The imported consignment is detained at the border until laboratory results are completed. Due to the time-sensitivity of such imports, the samples are usually only inspected or tested for the taxa of concern.

    2.

    Audit samples. As above, these samples are drawn from consignments of plant products for immediate use. However, they are drawn on an ad hoc (haphazard) basis from consignments that show no signs of contamination during border inspections. In the laboratory, these samples are often inspected or tested for multiple taxa.

    3.

    Post-entry quarantine (PEQ) samples. Plant products for propagation purposes or nursery material (e.g. in vitro plantlets, seedlings, budwood) are shipped in sealed packages and transported directly to DALRRD’s agricultural quarantine facilities. For small consignments (under 50 units), all units in the consignment are tested and inspected by laboratory officials. For larger consignments, random samples are drawn and inspected following a hypergeometric sampling protocol11. Inspection for arthropods and initial examination for micro-organisms takes place in a biosecurity containment facility (see Saccaggi & Pieterse12 for further details). The material is then grown in a dedicated quarantine facility and further testing for pathogens takes place when the plants are in active growth.

    Fig. 1Summary of border and laboratory processes associated with each of the three import sample sources included in this dataset, namely post-entry quarantine (PEQ), intervention and audit samples. Solid lines indicate that these processes are always followed, while dashed lines indicate that the process is sometimes followed. PEQ samples are received from plant propagation or nursery material that needs to be quarantined upon arrival. Intervention samples are received from consignments in which the border inspector finds or suspects a pest or pathogen. Audit samples are ad hoc samples drawn from consignments that show no sign of contamination. These sample sources are explained in more detail in the text.Full size imageTaxa inspection, testing and identification methodsAll inspections, testing and identifications are carried out by DALRRD laboratory officials specialised in each taxonomic group. Taxonomic identifications are routinely done by DALRRD officials, taxonomists at the Biosystematics Division of the South African Agricultural Research Council (ARC) or higher education institutions, depending on the expertise available at the time. All recorded identifications in the dataset were retained, regardless of level of identification or biosecurity status of the organism. It should, however, be noted that all organisms found were not always recorded (see below for further explanation).Arthropods (mostly insects and mites) and Molluscs are detected via visual inspection using a stereo-microscope. For these taxa, all organisms detected are recorded. Organisms are most commonly identified morphologically, with molecular identification being performed for certain groups. Identification is performed to the point at which a reasonable phytosanitary decision can be made (i.e. sometimes taxonomic precision is sacrificed for time and/or resource efficiency and logistic reasons). Thus specimens from predatory or saprophytic groups are often only identified to family or genus, while specimens within plant-feeding groups are identified to species where possible.Nematodes are detected by extraction from samples using relevant extraction methods. Saprophytic and predatory nematodes are sometimes noted, but often ignored as they are not considered to be of phytosanitary concern. Plant-feeding nematodes are identified morphologically to species where possible.Fungi and Bacteria are detected visually in the growing plant, as well as by conventional isolation and plating techniques, followed by biochemical tests and/or morphological identification. Some targeted pathogens are detected and identified by molecular techniques such as PCR and DNA sequencing. Saprophytic or secondary fungi or bacteria are sometimes noted, but often not recorded as part of the sample record.Viruses are screened for by immunological techniques, notably ELISA and hardwood and herbaceous indexing. ELISA techniques detect a target virus of concern and give no information as to the presence or absence of other viruses in the sample. Hardwood and herbaceous indexing are used to determine if any graft- or mechanically-transmissible viruses are present in the sample, although these methods cannot be used to determine the viruses’ identity.Phytoplasma screening is done by nested PCR designed to detect any phytoplasma. On specific crops, phytoplasma groups are detected by using targeted PCR methods. If necessary, sequencing of PCR products is used for more specific identification.Data collection and handlingMetadata for samples were recorded by the border inspector before submission to DALRRD’s laboratories. Ideally, he/she recorded geographic origin of the commodity, crop and sample type, date of collection, details of importer and exporter, organisms to test for and any additional observations. However, in practice, this information was not always recorded in full. See Tables 1, 2 and 3 for more details on information included in the dataset. Due to the sensitivity of this kind of trade data, some of the data in the current dataset are grouped or anonymised to protect confidentiality. In particular, import date is only listed as month and year and the names of importers and exporters are removed.Table 1 A summary of information fields and descriptions for each imported sample recorded in the South African plant import dataset used in the datasheet “List of contaminants on SA plant imports 1994–2019.csv”23.Full size tableTable 2 Information fields and descriptions for taxa information associated with contaminant organisms detected on import samples received by South Africa used in the datasheet “Metadata of contaminants on SA plant imports 1994–2019.csv”23.Full size tableTable 3 List of import commodity types used in the datasheet “List of contamiants on SA plant imports 1994–2019.csv”23. The original categories listed by the inspectors were expanded to 30 commodity types based on additional laboratory information and expert experience.Full size tableElectronic databases of samples received by the DALRRD laboratories were maintained by the laboratory staff. These databases were not official departmental databases and therefore did not need to include information relevant to other sections involved in biosecurity. For instance, total number of imports, total size of each consignment, observations of the inspector, details of phytosanitary certificates and release or detention of the consignment were never recorded. The databases also included samples processed by the laboratory for export or for national pest surveys. Partly due to their unofficial status, the databases were transient, with new databases started once software became outdated, the old one became too big or when new categories or information were to be included. For this study, we collated, curated and cross-checked information from nine of these databases, spanning 26 years from 1994 to 2019.Recorded laboratory data varied between taxa and over time and as priorities and understanding of biosecurity changed. In the initial years considered here (ca. 1994–2000), the focus was on pests or pathogens of quarantine importance, i.e. those on the prohibited list. Other organisms found on samples were not consistently recorded and, when they were, they were often recorded in broad groupings (e.g. “saprophytic nematodes”). More recently, there has been a shift towards recording all organisms detected, but this has still not been done consistently [although from ~2005 onwards the officials responsible for arthropods and molluscs have tried to record everything found (DS, MA personal observations)]. Thus prohibited (i.e. quarantine organisms) were always recorded, but the recording of other contaminants was inconsistent.Data clean-up started with collation of all data from the nine databases. Initially, these contained 99,023 records, with 50,655 recorded as imports, 31,163 as exports, 11,004 as surveys with the remaining 6,201 falling into other categories or uncategorised. Only imports were retained, as this was the only category of interest for this study. For some imports, sample information was recorded in one database, while results of inspections/tests for different taxa were recorded in other databases. Thus a single sample could have up to four duplicate records. Each of these was checked individually and collated into one record for the sample. Spelling mistakes, incorrectly recorded information (e.g. information recorded in the wrong field) and missing information were traced back through paper records and corrected wherever possible. If the original data could not be found, these ambiguous records were excluded. After this data clean-up, the dataset comprised a list of 26,291 import records, of which 2,572 resulted from intervention samples (sample source 1 above, Fig. 1), 10,629 were audit samples (sample source 2 above, Fig. 1) and 13,090 were PEQ samples (sample source 3 above, Fig. 1). Data clean-up then continued for the organisms found on the imported samples.Taxon names were extracted and spelling and classification were corrected and/or added by hand. The list of taxa was checked against the Global Biodiversity Information Facility (GBIF)13 using the software package ‘rgbif’14 in Rstudio version 1.3.95915 running R version 4.0.216. This highlighted additional spelling mistakes and provided a taxonomic backbone to work from. The classification of a number of taxa had changed over the years and thus using a common taxonomic backbone was needed for consistency. Some taxa, most notably some mite species, could not be found on GBIF. In these cases, the taxonomy provided by the taxonomist who initially identified the organism was retained. Virus taxonomic information was also not available on GBIF and the database of the International Committee on Taxonomy of Viruses (ICTV) was used17.Species occurrence in South Africa was determined by consulting published species distribution lists. The following data sources were consulted: GBIF13 (accessed 29 July and 03 Aug 2020); CABI Crop Pest Compendiums and Invasive Species Compendium18,19,20; the Catalogue of Life21; animal species checklists published by the South African Biodiversity Institute (SANBI)22; and for any remaining species internet searches were conducted for literature citing distributions (listed in Table 2).In South Africa, lists of organisms prohibited from entering the country have been compiled by DALRRD and the Department of Forestry, Fisheries and the Environment (DFFtE). DFFtE’s list of prohibited species focussed mostly on organisms of environmental concern, although some prohibited organisms were also of agricultural concern, while DALRRD is only concerned with agricultural pests. DALRRD issues import permits for each unique crop, commodity and country combination from which plant products originate. Thus there is no single consolidated quarantine list for South Africa. Furthermore, any quarantine list is not static, but needs to change as species’ distributions, taxonomic revisions or pest status changes. Thus it is very difficult to provide a list of which detected organisms are of quarantine status to South Africa at any given time and particularly in a dataset spanning 26 years. As far as possible, we have indicated the regulatory status of the species in the datasheet “Metadata of contaminants on SA plant imports 1994–2019.csv”23. This regulatory status would have been of critical importance to inform contemporary phytosanitary decisions. However, given that such lists are dynamic and a core aim of presenting these data is to facilitate analyses of future invaders9, it is important to present information on all organisms detected. Moreover, this allows a more comprehensive assessment of the role of different pathways and will facilitate comparisons with other countries. More

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    Benthic and coral reef community field data for Heron Reef, Southern Great Barrier Reef, Australia, 2002–2018

    This study describes a unique point-based data set for coral reef environments, collected using a photoquadrat survey method published for seagrass environments1. The data set describes the spatial and temporal distribution of benthic community abundance and composition for Heron Reef, a 28 km2 shallow platform reef located in the Capricorn Bunker Group, Southern Great Barrier Reef (GBR), Australia. On average, 3,600 coral reef data points were collected annually over the period 2002 to 2018. Annual data sets were acquired for independent research projects, but the collection methods were consistent. The initial field data collection design was planned to acquire detailed field data to describe the spatial distribution and variability of benthic composition across the study site to assist with calibration and validation of earth observation-based mapping products.To create a map based on earth observation imagery, it is common to use training or calibration data to transform the imagery into a map of surface properties using a supervised algorithm (e.g. multivariate statistical clustering, random forest)2. To report on the accuracy measures of the maps, reference or validation data are contrasted with the output maps3. Hence for calibration and validation purposes, georeferenced field data must be representative of all the features to be mapped and collection should ideally coincide with satellite image acquisition. Many earth observation approaches have been implemented for mapping the benthic communities of Heron Reef4,5,6,7,8,9,10,11,12 and several of these maps are now accessible online6,13,14.Several studies have utilised time series benthic data to analyse changes in benthic community and coral type trends, supporting broad ecological knowledge of coral reef ecosystems such as the Caribbean reef degradation15 and coral cover decline on the GBR16. Similarly, benthic community and coral cover data sets have been identified as important indicators of coral reef health providing the backbone for monitoring and management initiatives around the world17,18.Articles and data sets have been published that describe the benthic community properties of Heron Reef, however, their spatial coverage, number of georeferenced data points, and revisit times are limited19. The time series photoquadrat data sets presented in this paper could be used for further understanding of benthic community distribution, including statistical analysis of trends in coral cover, analysis of changes in benthic community and coral type, or used for testing of other earth observation-based mapping and modelling approaches. Additionally, as our methodology describes machine annotation of the field photoquadrats, it would be possible to reanalyse the photoquadrats with new categories not previously considered important from a biological perspective (e.g. unknown disease or impact, or a specific benthic community type), or for other features (e.g. the counting of sea cucumbers (Holothuroidea sp.)).Detailed analyses of our complete data set may permit a greater understanding of the persistence and/or dynamics of the benthic community at Heron Reef. As such, our ongoing analyses include evaluation of changes in community composition following major impacts such as cyclones, coral bleaching, crown of thorns predation, etc., and additionally, statistical analyses of coral recovery after such impacts. To this degree, these benthic community data sets are invaluable. More

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    Sedimentary ancient DNA as a tool in paleoecology

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    Oviposition behavior of wild yellow fever vector mosquitoes (Diptera: Culicidae) in an Atlantic Forest fragment, Rio de Janeiro state, Brazil

    1.Alho, C. J. R. Importância da biodiversidade para a saúde humana: uma perspectiva ecológica. Estud. Avançados 26, 151–166 (2012).Article 

    Google Scholar 
    2.Docile, T. N., Figueiró, R., Portela, C. & Nessimian, J. L. Macroinvertebrate diversity loss in urban streams from tropical forests. Environ. Monit. Assess. https://doi.org/10.1007/s10661-016-5237-z (2016).Article 
    PubMed 

    Google Scholar 
    3.Mutuku, F. M. et al. Distribution, description, and local knowledge of larval habitats of Anopheles gambiae s.l. in a village in western Kenya. Am. J. Trop. Med. Hyg. 74, 44–53 (2006).Article 

    Google Scholar 
    4.Simard, F. et al. Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation. BMC Ecol. 9, 17 (2009).Article 

    Google Scholar 
    5.Reiter, P. Yellow fever and dengue: a threat to Europe?. Eurosurveillance 15, 11–17 (2010).
    Google Scholar 
    6.Medlock, J. M. & Leach, S. A. Effect of climate change on vector-borne disease risk in the UK. Lancet Infect. Dis. 15, 721–730 (2015).Article 

    Google Scholar 
    7.Alencar, J. et al. Ecosystem diversity of mosquitoes (Diptera: Culicidae) in a remnant of Atlantic Forest, Rio de Janeiro state, Brazil . Austral Entomol. https://doi.org/10.1111/aen.12508 (2020).Article 

    Google Scholar 
    8.Arnell, J. H. Mosquito studies (Diptera, Culicidae). XXXII. A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst. 10, 1–174 (1973).
    Google Scholar 
    9.Alencar, J. et al. Flight height preference for oviposition of mosquito (diptera: Culicidae) vectors of sylvatic yellow fever virus near the hydroelectric reservoir of simplicío, minas Gerais, Brazil. J. Med. Entomol. 50, 791–795 (2013).Article 

    Google Scholar 
    10.Alencar, J. et al. Diversity of yellow fever mosquito vectors in the Atlantic forest of Rio de Janeiro, Brazil . Rev. Soc. Bras. Med. Trop. 49, 351–356 (2016).Article 

    Google Scholar 
    11.Gerais, M. Febre Amarela : uma visão do cenário atual. (2014).12.De Abreu, F. V. S. et al. Combination of surveillance tools reveals that yellow fever virus can remain in the same atlantic forest area at least for three transmission seasons. Mem. Inst. Oswaldo Cruz https://doi.org/10.1590/0074-02760190076 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Moreno, E. S. et al. Reemergência de febre amarela: Detecção de transmissão no estado de São Paulo, Brasil, 2008. Rev. Soc. Bras. Med. Trop. 44, 290–296 (2011).Article 

    Google Scholar 
    14.Bergallo, H. Estratégias e ações para a conservação da biodiversidade no estado do Rio de Janeiro. (Instituto Biomas, 2009).15.Silva, S. O. F. et al. Evaluation of multiple immersion effects on eggs from Haemagogus leucocelaenus, Haemagogus janthinomys, and Aedes albopictus (Diptera: Culicidae) under experimental conditions. J. Med. Entomol. 55, 1093–1097 (2018).Article 

    Google Scholar 
    16.Forattini, O. P. Culicidologia Médica: Identificação, Biologia, Epidemiologia. (Edusp – Editora da Universidade de São Paulo, 2002).17.Marcondes, C. & Alencar, J. Revisão de mosquitos Haemagogus Williston (Diptera: Culicidae) do Brasil. Rev. Biomed. 21, 221–238 (2010).
    Google Scholar 
    18.Reinert, J. F. Revised list of abbreviations for genera and subgenera of Culicidae (diptera) and notes on generic and subgeneric changes. J. Am. Mosq. Control Assoc. 17, 51–55 (2001).CAS 
    PubMed 

    Google Scholar 
    19.Guimaráes, A. É., De Mello, R. P., Lopes, C. M. & Gentile, C. Ecology of mosquitoes (Diptera: Culicidae) in areas of Serra do Mar State Park, State of São Paulo, Brazil. I—monthly frequency and climatic factors. Mem. Inst. Oswaldo Cruz 95, 1–16 (2000).Article 

    Google Scholar 
    20.Gratz, N. G. Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. 18, 215–227 (2004).CAS 
    Article 

    Google Scholar 
    21.Possas, C. et al. Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation. Mem. Inst. Oswaldo Cruz 113, e180278 (2018).Article 

    Google Scholar 
    22.Brasil, M. da S. Uma análise da situação de saúde com enfoque nas doenças imunopreveníveis e na imunização. Ministário da Saúde https://bvsms.saude.gov.br/bvs/saudelegis/gm/1998/prt3916_30_10_1998.htmlhttp://bvsms.saude.gov.br/bvs/saudelegis/gm/2017/prt2436_22_09_2017.html (2019).23.Cunha, M. S. et al. Epizootics due to Yellow Fever Virus in São Paulo State, Brazil: viral dissemination to new areas (2016–2017). Sci. Rep. 9, 1–13 (2019).ADS 

    Google Scholar 
    24.Lourenço-de-Oliveira, R. & Failloux, A. B. High risk for chikungunya virus to initiate an enzootic sylvatic cycle in the tropical Americas. PLoS Negl. Trop. Dis. 11, 1–11 (2017).
    Google Scholar 
    25.De Figueiredo, M. L. et al. Mosquitoes infected with dengue viruses in Brazil. Virol. J. 7, 1–5 (2010).Article 

    Google Scholar 
    26.Marcondes, C. B. & de Ximenes, M. F. F. M. Zika virus in Brazil and the danger of infestation by aedes (Stegomyia) mosquitoes. Rev. Soc. Bras. Med. Trop. 49, 4–10 (2016).Article 

    Google Scholar 
    27.Grard, G. et al. Zika virus in Gabon (Central Africa) – 2007: a new threat from Aedes albopictus?. PLoS Negl. Trop. Dis. 8, 1–6 (2014).ADS 
    Article 

    Google Scholar 
    28.de Gomes, A. C. et al. Aedes albopictus em área rural do Brasil e implicações na transmissão de febre amarela silvestre. Rev. Saude Publica 33, 95–97 (1999).Article 

    Google Scholar 
    29.Guimarães, A. E. Mosquitos no Parque Nacional da Serra dos Órgãos, Estado do Rio de Janeiro, Brasil. II. Distribuição vertical. Mem. Inst. Oswaldo Cruz 80, 1–2 (1985).MathSciNet 
    Article 

    Google Scholar 
    30.Lopes, J., Arias, J. R. & Yood, J. D. C. Evidências Preliminares De Estratificação Vertical De Postura De Ovos Por Alguns Culicidae (Diptera), Em Floresta No Município De Manaus – Amazonas. Acta Amaz. 13, 431–439 (1983).Article 

    Google Scholar 
    31.Alencar, J. et al. A comparative study of the effect of multiple immersions on Aedini (Diptera: Culicidae) mosquito eggs with emphasis on sylvan vectors of yellow fever virus. Mem. Inst. Oswaldo Cruz 109, 114–117 (2014).Article 

    Google Scholar 
    32.Entomologia médica. 2.O Volume. Culicini: Culex, Aedes e Psorophora | Mosquito Taxonomic Inventory. (1965).33.Principais Mosquitos de Importância Sanitária no Brasil – Fundação Oswaldo Cruz (Fiocruz): Ciência e tecnologia em saúde para a população brasileira. (FIOCRUZ, 1994).34.Amerasinghe, F. P. & Alagoda, T. S. B. Mosquito oviposition in bamboo traps, with special reference to Aedes albopictus, Aedes novalbopictus and Armigeres subalbatus. Int. J. Trop. Insect Sci. 5, 493–500 (1984).Article 

    Google Scholar 
    35.Obenauer, P. J., Kaufman, P. E., Allan, S. A. & Kline, D. L. Infusion-baited ovitraps to survey ovipositional height preferences of container-inhabiting mosquitoes in two Florida habitats. J. Med. Entomol. 46, 1507–1513 (2009).CAS 
    Article 

    Google Scholar 
    36.Althouse, B. M. et al. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. PLoS Negl. Trop. Dis. 10, 1–11 (2016).Article 

    Google Scholar 
    37.Hamrick, P. N. et al. Geographic patterns and environmental factors associated with human yellow fever presence in the Americas. PLoS Negl. Trop. Dis. 11, 1–27 (2017).Article 

    Google Scholar 
    38.Couto-Lima, D. et al. Seasonal population dynamics of the primary yellow fever vector haemagogus leucocelaenus (Dyar & shannon) (diptera: Culicidae) is mainly influenced by temperature in the atlantic forest, Southeast Brazil. Mem. Inst. Oswaldo Cruz 115, 1–13 (2020).Article 

    Google Scholar 
    39.Davis, N. C., Division, I. H., Foundation, R., Health, P. & Health, P. The effect of various temperatures in modifying the extrinsic incubation period of the yellow fever virus in Aedes Aegypti. Am. J. Epidemiol. 16, 163–176 (1931).Article 

    Google Scholar 
    40.Johansson, M. A., Arana-Vizcarrondo, N., Biggerstaff, B. J. & Staples, J. E. Incubation periods of yellow fever virus. Am. J. Trop. Med. Hyg. 83, 183–188 (2010).Article 

    Google Scholar 
    41.De Paiva, C. A. et al. Determination of the spatial susceptibility to yellow fever using a multicriteria analysis. Mem. Inst. Oswaldo Cruz 114, 1–8 (2019).Article 

    Google Scholar 
    42.Calado, D. C. & Navarro da Silva, M. A. Evaluation of the temperature influence on the development of Aedes albopictus. Rev. Saude Publica 36, 173–179 (2002).Article 

    Google Scholar 
    43.Docile, T. N. et al. Frequency of Aedes sp. Linnaeus (Diptera: Culicidae) and Associated Entomofauna in Bromeliads from a Forest Patch within a densely Urbanized Area. Neotrop. Entomol. 46, 613–621 (2017).CAS 
    Article 

    Google Scholar  More

  • in

    Impact of artificial light at night on diurnal plant-pollinator interactions

    1.Falchi, F. et al. The new world atlas of artificial night sky brightness. Sci. Adv. 2, e1600377 (2016).ADS 
    Article 

    Google Scholar 
    2.Kyba, C. C. et al. Artificially lit surface of earth at night increasing in radiance and extent. Sci. Adv. 3, e1701528 (2017).ADS 
    Article 

    Google Scholar 
    3.Longcore, T. & Rich, C. Ecological light pollution. Front. Ecol. Environ. 2, 191–198 (2004).Article 

    Google Scholar 
    4.Rich, C. & Longcore, T. Ecological Consequences of Artificial Night Lighting, (Island Press, 2013).5.Davies, T. W., Bennie, J. & Gaston, K. J. Street lighting changes the composition of invertebrate communities. Biol. Lett. rsbl20120216 8, 764–767 (2012).6.Gaston, K. J. & Bennie, J. Demographic effects of artificial nighttime lighting on animal populations. Environ. Rev. 22, 323–330 (2014).Article 

    Google Scholar 
    7.Desouhant, E., Gomes, E., Mondy, N. & Amat, I. Mechanistic, ecological, and evolutionary consequences of artificial light at night for insects: review and prospective. Entomologia Experimentalis et Applicata 167, 37–58 (2019).Article 

    Google Scholar 
    8.Sanders, D. & Gaston, K. J. How ecological communities respond to artificial light at night. J. Exp. Zool. Part A: Ecol. Integr. Physiol. 329, 394–400 (2018).
    Google Scholar 
    9.Dwyer, R. G., Bearhop, S., Campbell, H. A. & Bryant, D. M. Shedding light on light: benefits of anthropogenic illumination to a nocturnally foraging shorebird. J. Anim. Ecol. 82, 478–485 (2013).Article 

    Google Scholar 
    10.Blake, D., Hutson, A. M., Racey, P. A., Rydell, J. & Speakman, J. R. Use of lamplit roads by foraging bats in southern England. J. Zool. 234, 453–462 (1994).Article 

    Google Scholar 
    11.Polak, T., Korine, C., Yair, S. & Holderied, M. W. Differential effects of artificial lighting on flight and foraging behaviour of two sympatric bat species in a desert. J. Zool. 285, 21–27 (2011).
    Google Scholar 
    12.Spoelstra, K. et al. Response of bats to light with different spectra: Light-shy and agile bat presence is affected by white and green, but not red light. Proc. R. Soc. B: Biol. Sci. 284, 11–15 (2017).Article 

    Google Scholar 
    13.Straka, T. M., Wolf, M., Gras, P., Buchholz, S. & Voigt, C. C. Tree cover mediates the effect of artificial light on urban bats. Front. Ecol. Evol. 7, 91 (2019).Article 

    Google Scholar 
    14.Heiling, A. M. Why do nocturnal orb-web spiders (Araneidae) search for light? Behav. Ecol. 46, 43–49 (1999).Article 

    Google Scholar 
    15.Bennie, J., Davies, T. W., Cruse, D., Inger, R. & Gaston, K. J. Artificial light at night causes top-down and bottom-up trophic effects on invertebrate populations. J. Appl. Ecol. 55, 2698–2706 (2018).CAS 
    Article 

    Google Scholar 
    16.Grenis, K. & Murphy, S. M. Direct and indirect effects of light pollution on the performance of an herbivorous insect. Insect Sci. 26, 770–776 (2019).Article 

    Google Scholar 
    17.McMunn, M. S. et al. Artificial light increases local predator abundance, predation rates, and herbivory. Environ. Entomol. 48, 1331–1339 (2019).Article 

    Google Scholar 
    18.Giavi, S., Blösch, S., Schuster, G. & Knop, E. Artificial light at night can modify ecosystem functioning beyond the lit area. Sci. Rep. 10, 1–11 (2020).Article 

    Google Scholar 
    19.Knop, E. et al. Artificial light at night as a new threat to pollination. Nature 548, 206–209 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    20.Macgregor, C. J., Evans, D. M., Fox, R. & Pocock, M. J. O. The dark side of street lighting: impacts on moths and evidence for the disruption of nocturnal pollen transport. Glob. Change Biol. 23, 697–707 (2017).ADS 
    Article 

    Google Scholar 
    21.Macgregor, C. J., Pocock, M. J. O., Fox, R. & Evans, D. M. Effects of street lighting technologies on the success and quality of pollination in a nocturnally pollinated plant. Ecosphere 10, 1–16 (2019).22.Junker, R. R. et al. Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct. Ecol. 27, 329–341 (2013).Article 

    Google Scholar 
    23.Bennie, J., Duffy, J. P., Davies, T. W., Correa-Cano, M. E. & Gaston, K. J. Global trends in exposure to light pollution in natural terrestrial ecosystems. Remote Sens. 7, 2715–2730 (2015).ADS 
    Article 

    Google Scholar 
    24.Bennie, J., Davies, T. W., Cruse, D. & Gaston, K. J. Ecological effects of artificial light at night on wild plants. J. Ecol. 104, 611–620 (2016).Article 

    Google Scholar 
    25.Bloch, G., Bar-Shai, N., Cytter, Y. & Green, R. Time is honey: circadian clocks of bees and flowers and how their interactions may influence ecological communities. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20160256 (2017).26.Yon, F. et al. Fitness consequences of altering floral circadian oscillations for Nicotiana attenuata. J. Integr. Plant Biol. 59, 180–189 (2017).CAS 
    Article 

    Google Scholar 
    27.Yon, F., Kessler, D., Joo, Y., Kim, S.-G. & Baldwin, I. T. Fitness consequences of a clock pollinator filter in Nicotiana attenuata flowers in nature. J. Integr. Plant Biol. 59, 805–809 (2017).CAS 
    Article 

    Google Scholar 
    28.Fenske, M. P., Nguyen, L. A. P., Horn, E. K., Riffell, J. A. & Imaizumi, T. Circadian clocks of both plants and pollinators influence flower seeking behavior of the pollinator hawkmoth Manduca sexta. Sci. Rep. 8, 1–13 (2018).CAS 
    Article 

    Google Scholar 
    29.Rusman, Q., Lucas-Barbosa, D. & Poelman, E. H. Dealing with mutualists and antagonists: Specificity of plant-mediated interactions between herbivores and flower visitors, and consequences for plant fitness. Funct. Ecol. 32, 1022–1035 (2018).Article 

    Google Scholar 
    30.Rusman, Q., Lucas-Barbosa, D., Poelman, E. H. & Dicke, M. Ecology of plastic flowers. Trends Plant Sci. 24, 725–740 (2019).31.Barber, N. A., Adler, L. S., Theis, N., Hazzard, R. V. & Kiers, E. T. Herbivory reduces plant interactions with above-and belowground antagonists and mutualists. Ecology 93, 1560–1570 (2012).Article 

    Google Scholar 
    32.Liao, K., Gituru, R. W., Guo, Y.-H. & Wang, Q.-F. Effects of floral herbivory on foraging behaviour of bumblebees and female reproductive success in Pedicularis gruina (Orobanchaceae). Flora – Morphol., Distrib., Funct. Ecol. Plants 208, 562–569 (2013).Article 

    Google Scholar 
    33.Schiestl, F. P., Kirk, H., Bigler, L., Cozzolino, S. & Desurmont, G. A. Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. N. Phytologist 203, 257–266 (2014).CAS 
    Article 

    Google Scholar 
    34.Jacobsen, D. J. & Raguso, R. A. Lingering effects of herbivory and plant defenses on pollinators. Curr. Biol. 28, R1164–R1169 (2018).CAS 
    Article 

    Google Scholar 
    35.Barber, N. A., Adler, L. S. & Bernardo, H. L. Effects of above-and belowground herbivory on growth, pollination, and reproduction in cucumber. Oecologia 165, 377–386 (2011).ADS 
    Article 

    Google Scholar 
    36.Poveda, K., Steffan-Dewenter, I., Scheu, S. & Tscharntke, T. Effects of below-and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135, 601–605 (2003).ADS 
    Article 

    Google Scholar 
    37.Ivey, C. T. & Carr, D. E. Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). Am. J. Bot. 92, 1641–1649 (2005).Article 

    Google Scholar 
    38.Lucas-Barbosa, D. et al. Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Funct. Ecol. 30, 431–441 (2016).Article 

    Google Scholar 
    39.Dominoni, D. M. & Partecke, J. Does light pollution alter daylength? A test using light loggers on free-ranging European blackbirds (Turdus merula). Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 370, 20140118 (2015).40.Davies, T. W. & Smyth, T. Why artificial light at night should be a focus for global change research in the 21st century. Glob. Change Biol. 24, 872–882 (2018).ADS 
    Article 

    Google Scholar 
    41.Sage, R. F. Global change biology: a primer. Global Change Biol. 26, 3–30 (2019).42.Gibson, R. H., Knott, B., Eberlein, T. & Memmott, J. Sampling method influences the structure of plant-pollinator networks. Oikos 120, 822–831 (2011).Article 

    Google Scholar 
    43.R Core Team. R: a language and environment for statistical computing. (R Foundation for Statistical Computing, 2020).44.Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using {lme4}. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar 
    45.Giavi, S., Fontaine, C., Knop, E. Data and code for ‘Impact of artificial light at night on diurnal plant-pollinator interactions’ (Version v1) [Data set and data code]. Zenodo https://zenodo.org/record/4540407#.YCqYPTKg82w (2021). More

  • in

    Conspicuousness, phylogenetic structure, and origins of Müllerian mimicry in 4000 lycid beetles from all zoogeographic regions

    1.Müller, F. Ituna and Thyridia: A remarkable case of mimicry in butterflies. Proc. Entomol. Soc. Lond. 1879, 20–24 (1879).
    Google Scholar 
    2.Mallet, J. & Joron, M. Evolution of diversity in warning color and mimicry: Polymorphisms, shifting balance, and speciation. Ann. Rev. Ecol. Evol. Syst. 30, 201–233 (1999).Article 

    Google Scholar 
    3.Sherratt, T. N. The evolution of Müllerian mimicry. Naturwissenschaften 95, 681–695 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Beatty, C. D., Beirinckx, K. & Sherratt, T. N. The evolution of Müllerian mimicry in multispecies communities. Nature 431, 63–67 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Mallet, L. & Barton, N. H. Strong natural selection in a warning colour hybrid zone. Evolution 43, 421–431 (1989).PubMed 
    Article 

    Google Scholar 
    6.Chouteau, M., Arias, M. & Joron, M. Warning signals are under positive frequency-dependent selection in nature. Proc. Natl. Acad. Sci. USA 113, 2164–2169 (2016).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Wilson, J. S., Williams, K. A., Forister, M. L., von Dohlen, C. D. & Pitts, J. P. Repeated evolution in overlapping mimicry rings among North American velvet ants. Nat. Commun. 3, 1272. https://doi.org/10.1038/ncomms2275 (2012).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    8.Wilson, J. S. et al. North American velvet ants form one of the world’s largest known Mullerian mimicry complexes. Curr. Biol. 25, R704–R706. https://doi.org/10.1016/j.cub.2015.06.053 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    9.Bocek, M., Kusy, D., Motyka, M. & Bocak, L. Persistence of multiple patterns and intraspecific polymorphism in multi-species Müllerian communities of net-winged beetles. Front. Zool. 16, 38. https://doi.org/10.1186/s12983-019-0335-8 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    10.Anzaldo, S. S., Wilson, J. S. & Franz, N. M. Phenotypic analysis of aposematic conoderine weevils (Coleoptera: Curculionidae: Conoderinae) supports the existence of three large mimicry complexes. Biol. J. Linn. Soc. 129, 728–739 (2020).Article 

    Google Scholar 
    11.Masek, M. et al. Molecular phylogeny, diversity and zoogeography of net-winged beetles (Coleoptera: Lycidae). Insects 9, 154. https://doi.org/10.3390/insects9040154 (2018).Article 
    PubMed Central 
    PubMed 

    Google Scholar 
    12.Kusy, D., Motyka, M., Bocek, M., Vogler, A. P. & Bocak, L. Genome sequences identify three families of Coleoptera as morphologically derived click beetles (Elateridae). Sci. Rep. 8, 17084. https://doi.org/10.1038/s41598-018-35328-0 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Linsley, E. G., Eisner, T. & Klots, A. B. Mimetic assemblages of sibling species of lycid beetles. Evolution 15, 15–29 (1961).Article 

    Google Scholar 
    14.Eisner, T., Kafatos, F. C. & Linsley, E. G. Lycid predation by mimetic adult Cerambycidae (Coleoptera). Evolution 16, 316–324 (1962).Article 

    Google Scholar 
    15.Dettner, K. Chemosystematics and evolution of beetle chemical defenses. Ann. Rev. Entomol. 32, 17–48 (1987).CAS 
    Article 

    Google Scholar 
    16.Malohlava, V. & Bocak, L. Evidence of extreme habitat stability in a Southeast Asian biodiversity hotspot based on the evolutionary analysis of neotenic net-winged beetles. Mol. Ecol. 19, 4800–4811 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    17.Kazantsev, S. V. & Telnov, D. A mimetic assemblage of net-winged beetles (Coleoptera: Lycidae) from West Papua. In Biodiversity, Biogeography and Nature Conservation in Wallacea and New Guinea, Vol III (eds Telnov, D. et al.) 363–370 (The Entomological Society of Latvia, 2017).
    Google Scholar 
    18.Sklenarova, K., Chesters, D. & Bocak, L. Phylogeography of poorly dispersing net-winged beetles: A role of drifting India in the origin of Afrotropical and Oriental fauna. PLoS One 8, e67957. https://doi.org/10.1371/journal.pone.0067957 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Li, Y., Gunter, N., Pang, H. & Bocak, L. DNA-based species delimitation separates highly divergent populations within morphologically coherent clades of poorly dispersing beetles. Zool. J. Linn. Soc. 175, 59–72 (2015).Article 

    Google Scholar 
    20.Masek, M., Palata, V., Bray, T. C. & Bocak, L. Molecular phylogeny reveals high diversity and geographic structure in Asian neotenic net-winged beetles Platerodrilus (Coleoptera: Lycidae). PLoS One 10, e0123855. https://doi.org/10.1371/journal.pone.0123855 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    21.Bocakova, M., Bocak, L., Gimmel, M. L., Motyka, M. & Vogler, A. P. Aposematism and mimicry in soft-bodied beetles of the superfamily Cleroidea (Insecta). Zool. Scr. 45, 9–21 (2016).Article 

    Google Scholar 
    22.Moore, B. P. & Brown, W. V. Identification of warning odour components, bitter principles and antifeedants in an aposematic beetle: Metriorrhynchus rhipidius (Coleoptera: Lycidae). Ins. Biochem. 1, 493–499 (1981).Article 

    Google Scholar 
    23.Eisner, T. et al. Defensive chemistry of lycid beetles and of mimetic cerambycid beetles that feed on them. Chemoecology 18, 109–119 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Kusy, D., Motyka, M., Bocek, M., Masek, M. & Bocak, L. Phylogenomic analysis resolves the relationships among net-winged beetles (Coleoptera: Lycidae) and reveals the parallel evolution of morphological traits. Syst. Entomol. 44, 911–925 (2019).Article 

    Google Scholar 
    25.Blum, M. S. & Sannasi, A. Reflex bleeding in the lampyrid Photinus pyralis: Defensive function. J. Insect Physiol. 20, 451–460 (1974).Article 

    Google Scholar 
    26.Xinhua, F., Ohba, N., Meyer-Rochow, V. B., Yuyong, W. & Chaoliang, L. Reflex-bleeding in the firefly Pyrocoelia pectoralis (Coleoptera: Lampyridae): Morphological basis and possible function. Coleopt. Bull. 60, 207–215 (2006).Article 

    Google Scholar 
    27.Meinwald, J., Meinwald, Y. C., Calmers, A. M. & Eisner, T. Dihydromatricaria acid: Acetylenic acid secreted by soldier beetle. Science 160, 890–892 (1968).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Moore, B. P. & Brown, W. V. Precoccinelline and related alcaloids in the Australian soldier beetle, Chauliognathus pulchellus (Coleoptera: Cantharidae). Ins. Biochem. 8, 393–395 (1978).CAS 
    Article 

    Google Scholar 
    29.Poinar, G. O. Jr., Marshall, C. J. & Buckley, R. One hundred million years of chemical warfare by insects. J. Chem. Ecol. 33, 1663–1669 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Rowe, C. & Guilford, T. The evolution of multimodal warning displays. Evol. Ecol. 13, 655–671 (1999).Article 

    Google Scholar 
    31.Young, D. K. & Fischer, R. L. The pupation of Calopteron terminale (Say) (Coleoptera: Lycidae). Coleopt. Bull. 26, 17–18 (1972).
    Google Scholar 
    32.Bocak, L. & Matsuda, K. Review of the immature stages of the family Lycidae (Insecta: Coleoptera). J. Nat. Hist 37, 1463–1507 (2003).Article 

    Google Scholar 
    33.Hall, D. W. & Branham, M. A. Aggregation of Calopteron discrepans (Coleoptera: Lycidae) larvae prior to pupation. Flor. Entomol. 91, 124–125 (2008).Article 

    Google Scholar 
    34.Gamberale, G. & Tullberg, B. S. Aposematism and gregariousness: The combined effect of group size and coloration on signal repellence. Proc. R. Soc. Lond. B Biol. Sci. 265, 889–894 (1998).Article 

    Google Scholar 
    35.Svadová, K., Exnerová, A. & Štys, P. Gregariousness as a defence strategy of moderately defended prey: Experiments with Pyrrhocoris apterus and avian predators. Behaviour 151, 1617–1640 (2014).Article 

    Google Scholar 
    36.Mitchell, R. F. et al. Evidence that cerambycid beetles mimic vespid wasps in odor as well as appearance. J. Chem. Ecol. 43, 75–83 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Speed, M. P. Warning signals, receiver psychology and predator memory. Anim. Behav. 60, 269–278 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Speed, M. P. Can receiver psychology explain the evolution of aposematism?. Anim. Behav. 61, 205–216 (2001).PubMed 
    Article 

    Google Scholar 
    39.Skelhorn, J., Holmes, G. G., Hossie, T. J. & Sherratt, T. N. Multicomponent deceptive signals reduce the speed at which predators learn that prey are profitable. Behav. Ecol. 27, 141–147 (2016).Article 

    Google Scholar 
    40.Motyka, M., Kampova, L. & Bocak, L. Phylogeny and evolution of Müllerian mimicry in aposematic Dilophotes: Evidence for advergence and size-constraints in evolution of mimetic sexual dimorphism. Sci. Rep. 8, 3744. https://doi.org/10.1038/s41598-018-22155-6 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Motyka, M., Bocek, M., Kusy, D. & Bocak, L. Interactions in multi-pattern Mullerian communities support origins of new patterns, false structures, imperfect resemblance and mimetic sexual dimorphism. Sci. Rep. 10, 11193. https://doi.org/10.1038/s41598-020-68027-w (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Bocak, L. & Yagi, T. Evolution of mimicry patterns in Metriorrhynchus (Coleoptera: Lycidae): The history of dispersal and speciation in southeast Asia. Evolution 64, 39–52 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Bray, T. C. & Bocak, L. Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains. Sci. Rep. 6, 33579. https://doi.org/10.1038/srep33579 (2016).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Jiruskova, A., Motyka, M., Bocek, M. & Bocak, L. The Malacca Strait separates distinct faunas of poorly-flying Cautires net-winged beetles. PeerJ 7, e6511. https://doi.org/10.7717/peerj.6511 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    45.Endler, J. A. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vis. Res. 31, 587–608 (1991).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Arenas, L. M., Troscianko, J. & Stevens, M. Color contrast and stability as key elements for effective warning signals. Front. Ecol. Evol. 2, 1–12 (2014).Article 

    Google Scholar 
    47.Mallet, J. & Gilbert, L. E. Why are there so many mimicry rings—correlations between habitats, behavior and mimicry in Heliconius butterflies. Biol. J. Linn. Soc. 55, 159–180 (1995).
    Google Scholar 
    48.CSIRO. The Insects of Australia (Melbourne University Press, 1991).
    Google Scholar 
    49.Lingafelter, S. W. Hispaniolan Hemilophini (Coleoptera, Cerambycidae, Lamiinae). ZooKeys 258, 53–83 (2013).Article 

    Google Scholar 
    50.Perger, R. & Santos-Silva, A. A new lycid-like species of Iarucanga Martins & Galileo, 1991 (Coleoptera, Cerambycidae, Lamiinae, Hemilophini) from the Bolivian Andes. J. Nat. Hist. 52, 2487–2495 (2018).Article 

    Google Scholar 
    51.Perger, R. & Santos-Silva, A. Addition to the known long-horned beetle fauna of the Bolivian Andes: A new lycid-like species of Mimolaia Bates, 1885 (Coleoptera, Cerambycidae, Lamiinae, Caliini). Zootaxa 4550, 295–300 (2019).PubMed 
    Article 

    Google Scholar 
    52.Eisner, T. et al. Antifeedant action of z-dihydromatricaria acid from soldier beetles (Chauliognathus spp.). J. Chem. Ecol. 7, 1149–1158 (1981).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Brown, W. V., Lacey, M. J. & Moore, B. P. Dihydromatricariate-based triglycerides, glyceride ethers, and waxes in the Australian soldier beetle, Chauliognathus lugubris (Coleoptera: Cantharidae). J. Chem. Ecol. 14, 411–423 (1988).CAS 
    PubMed 
    Article 

    Google Scholar 
    54.Machado, V., Araujo, A. M., Serrano, J. & Galián, J. Phylogenetic relationships and the evolution of mimicry in the Chauliognathus yellow-black species complex (Coleoptera: Cantharidae) inferred from mitochondrial COI sequences. Gen. Mol. Biol. 27, 55–60 (2004).CAS 
    Article 

    Google Scholar 
    55.Long, S. M. et al. Firefly flashing and jumping spider predation. Anim. Behav. 83, 81–86 (2012).Article 

    Google Scholar 
    56.Eisner, T., Goetz, M. A., Hill, D. E., Smedley, S. R. & Meinwald, J. Firefly “femmes fatales” acquire defensive steroids (lucibufagins) from their firefly prey. Proc. Natl. Acad. Sci USA 94, 9723–9728 (1997).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Exnerová, A. et al. Importance of color in the reaction of passerine predators to aposematic prey: Experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biol. J. Linn. Soc. 88, 143–153 (2006).Article 

    Google Scholar 
    58.Wuster, W. et al. Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proc. R. Soc. B Biol. Sci. 271, 2495–2499 (2004).Article 

    Google Scholar 
    59.Speed, M. P. & Ruxton, G. D. How bright and how nasty: Explaining diversity in warning signal strength. Evolution 61, 623–635 (2007).PubMed 
    Article 

    Google Scholar 
    60.Aronsson, M. & Gamberale-Stille, G. Importance of internal pattern contrast and contrast against the background in aposematic signals. Behav. Ecol. 20, 1356–1362 (2009).Article 

    Google Scholar 
    61.Endler, J. A. & Mappes, J. The current and future state of animal coloration research. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160352 (2017).Article 

    Google Scholar 
    62.Edmunds, M. Why are there good and poor mimics?. Biol. J. Linn. Soc. 70, 459–466 (2000).Article 

    Google Scholar 
    63.Speed, M. P. & Ruxton, G. D. Imperfect Batesian mimicry and the conspicuousness costs of mimetic resemblance. Am. Nat. 176, E1–E14 (2010).PubMed 
    Article 

    Google Scholar 
    64.Penney, H. D., Hassall, C., Skevington, J. H., Abbott, K. R. & Sherratt, T. N. A comparative analysis of the evolution of imperfect mimicry. Nature 483, 461–464 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Kikuchi, D. W. & Pfennig, D. W. Imperfect mimicry and the limits of natural selection. Q. Rev. Biol. 88, 297–315 (2013).PubMed 
    Article 

    Google Scholar 
    66.Briolat, E. S. et al. Diversity in warning coloration: Selective paradox or the norm?. Biol. Rev. 94, 388–414 (2019).PubMed 
    Article 

    Google Scholar 
    67.Robertson, A. R. The CIE 1976 color-difference formulae. Color Res. Appl. 2, 7–11 (1976).Article 

    Google Scholar 
    68.Bocak, L., Bocakova, M., Hunt, T. & Vogler, A. P. Multiple ancient origins of neoteny in Lycidae (Coleoptera): Consequences for ecology and macroevolution. Proc. R. Soc. B Biol. Sci. 275, 2015–2023 (2008).Article 

    Google Scholar 
    69.Bocak, L., Kundrata, R., Andújar-Fernández, C. & Vogler, A. P. The discovery of Iberobaeniidae (Coleoptera: Elateroidea): A new family of beetles from Spain, with immatures detected by environmental DNA sequencing. Proc. R. Soc. B Biol. Sci. 283, 20152350 (2016).Article 
    CAS 

    Google Scholar 
    70.Bininda-Emonds, O. R. P. transAlign: Using amino acids to facilitate the multiple alignment of protein coding DNA sequences. BMC Bioinform. 6, 156 (2005).Article 
    CAS 

    Google Scholar 
    71.Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Kück, P. & Longo, G. C. FASconCAT-G: Extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Front. Zool. 11, 81 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).CAS 
    Article 

    Google Scholar 
    75.Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    76.Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Brower, A. V. Z. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial-DNA evolution. Proc. Natl. Acad. Sci. USA 91, 6491–6495 (1994).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    78.Papadopoulou, A., Anastasiou, I. & Vogler, A. P. Revisiting the insect mitochondrial molecular clock: The Mid-Aegean trench calibration. Mol. Biol. Evol. 27, 1659–1672 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Bocak, L., Li, Y. & Ellenberger, S. The discovery of Burmolycus compactus gen. et sp. Nov. from the mid-Cretaceous of Myanmar provides the evidence for early diversification of net-winged beetles (Coleoptera, Lycidae). Cret. Res. 99, 149–155 (2019).Article 

    Google Scholar 
    80.Molino-Olmedo, F., Ferreira, V. S., Branham, M. A. & Ivie, M. A. The description of Prototrichalus gen. nov. and three new species from Burmese amber supports a mid-Cretaceous origin of the Metriorrhynchini (Coleoptera, Lycidae). Cret. Res. 111, 104452 (2020).Article 

    Google Scholar 
    81.Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Borges, R., Machado, J. P., Gomes, C., Rocha, A. P. & Antunes, A. Measuring phylogenetic signal between categorical traits and phylogenies. Bioinformatics 35, 1862–1869 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    83.Paradis, E. & Schliep, K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Kusy, D., Sklenarova, K. & Bocak, L. The effectiveness of DNA-based delimitation in Synchonnus net-winged beetles (Coleoptera: Lycidae) assessed, and description of 11 new species. Austral. Entomol. 57, 25–39 (2018).Article 

    Google Scholar 
    85.Kusy, D. et al. Sexually dimorphic characters and shared aposematic patterns mislead the morphology-based classification of the Lycini (Coleoptera: Lycidae). Zool. J. Linn. Soc. https://doi.org/10.1093/zoolinnean/zlaa055 (2021).Article 

    Google Scholar 
    86.Endler, J. A. Frequency-dependent predation, crypsis and aposematic coloration. Philos. Trans. R. Soc. Lond. B Biol. Sci. 319, 505–523 (1988).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Guilford, T. The evolution of conspicuous coloration. Am. Nat. 131, S7–S21 (1988).Article 

    Google Scholar 
    88.Gamberalle-Stille, G. Benefit by contrast: An experiment with live aposematic prey. Behav. Ecol. 12, 768–772 (2001).Article 

    Google Scholar 
    89.Aronsson, M. & Gamberale-Stille, G. Evidence of signaling benefits to contrasting internal color boundaries in warning coloration. Behav. Ecol. 24, 349–354 (2013).Article 

    Google Scholar 
    90.Prudic, K. L., Skemp, A. K. & Papaj, D. R. Aposematic coloration, luminance contrast, and the benefits of conspicuousness. Behav. Ecol. 18, 41–46 (2007).Article 

    Google Scholar 
    91.van Hateren, J. H., Ruttiger, L., Sun, H. & Lee, B. B. Processing of natural temporal stimuli by macaque retinal ganglion cells. J. Neurosci. 22, 9945–9960 (2002).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    92.Bowdish, T. I. & Bultman, T. L. Visual cues used by mantids in learning aversion to aposematically colored prey. Am. Midl. Nat. 129, 215–222 (1993).Article 

    Google Scholar 
    93.Lindström, L., Alatalo, R. V., Lyytinen, A. & Mappes, J. Strong antiapostatic selection against novel rare aposematic prey. Proc. Natl. Acad. Sci. USA 98, 9181–9184 (2001).ADS 
    PubMed 
    Article 

    Google Scholar 
    94.Briscoe, A. D. & Chittka, L. The evolution of color vision in insects. Annu. Rev. Entomol. 46, 471–510 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    95.Fabricant, S. A. & Herberstein, M. E. Hidden in plain orange: Aposematic coloration is cryptic to a colorblind insect predator. Behav. Ecol. 26, 38–44 (2015).Article 

    Google Scholar 
    96.Nielsen, M. E. & Mappes, J. Out in the open: Behavior’s effect on predation risk and thermoregulation by aposematic caterpillars. Behav. Ecol. 31, 1031–1039 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Nokelainen, O., Valkonen, J., Lindstedt, C. & Mappes, J. Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths. J. Anim. Ecol. 83, 598–605 (2013).Article 

    Google Scholar 
    98.Guilford, T. How do “warning colours” work? conspicuousness may reduce recognition errors in experienced predators. Anim. Behav. 34, 286–288 (1986).Article 

    Google Scholar 
    99.Lovell, P. G. et al. Stability of the color-opponent signals under changes of illuminant in natural scenes. J. Opt. Soc. Am. A Opt. Imaging Sci. Vis. 22, 2060–2071 (2005).ADS 
    CAS 
    Article 

    Google Scholar 
    100.Rojas, B., Rautiala, P. & Mappes, J. Differential detectability of polymorphic warning signal under varying light environment. Behav. Proc. 109, 164–172 (2014).Article 

    Google Scholar 
    101.Fennell, J. G., Talas, L., Baddeley, R. J., Cuthill, I. C. & Scott-Samuel, N. E. Optimizing colour for camouflage and visibility using deep learning: The effects of the environment and the observer’s visual system. J. R. Soc. Interf. 16, 20190183. https://doi.org/10.1098/rsif.2019.0183 (2019).CAS 
    Article 

    Google Scholar 
    102.Marples, N. M., Roper, T. J. & Harper, D. G. C. Responses of wild birds to novel prey: Evidence of dietary conservatism. Oikos 83, 161–165 (1998).Article 

    Google Scholar 
    103.Siddiqi, A., Cronin, T. W., Loew, E. R., Vorobyev, M. & Summers, K. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J. Exp. Biol. 207, 2471–2485 (2004).PubMed 
    Article 

    Google Scholar 
    104.Endler, J. A. & Mielke, P. W. Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc. 86, 405–431 (2005).Article 

    Google Scholar 
    105.Bocak, L. & Bocakova, M. Revision of the supergeneric classification of the family Lycidae (Coleoptera). Pol. Pism. Entomol. 59, 623–676 (1990).
    Google Scholar 
    106.Bocak, L. & Bocakova, M. Phylogeny and classification of the family Lycidae (Insecta: Coleoptera). Ann. Zool 58, 695–720 (2008).Article 

    Google Scholar 
    107.Kazantsev, S. V. Morphology of Lycidae with some considerations on evolution of the Coleoptera. Elytron 17, 49–226 (2005).
    Google Scholar 
    108.Bocakova, M. Phylogeny and classification of the tribe Calopterini (Coleoptera, Lycidae). Inst. Syst. Evol. 35, 437–447 (2005).Article 

    Google Scholar 
    109.Eisner, T. et al. Chemical basis of courtship in a beetle (Neopyrochroa flabellata): Cantharidin as precopulatory “enticing” agent. Proc. Natl. Acad. Sci. USA 93, 6494–6498 (1996).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    110.Bocak, L. & Bocakova, M. Revision of the genus Dexoris C. O. Waterhouse (Coleoptera, Lycidae). Acta Entomol. Bohemoslov. 85, 194–204 (1988).
    Google Scholar 
    111.Bocak, L., Grebennikov, V. V. & Masek, M. A new species of Dexoris (Coleoptera: Lycidae) and parallel evolution of brachyptery in the soft-bodied elateroid beetles. Zootaxa 3721, 495–500 (2013).PubMed 
    Article 

    Google Scholar 
    112.True, J. R. Insect melanism: The molecules matter. Trend. Ecol. Evol. 18, 640–647 (2003).Article 

    Google Scholar 
    113.Shamim, G., Ranjan, S. K., Pandey, D. M. & Ramani, R. Biochemistry and biosynthesis of insect pigments. Eur. J. Entomol. 111, 149–164 (2014).CAS 
    Article 

    Google Scholar 
    114.Sillén-Tullberg, B. Evolution of gregariousness in aposematic butterfly larvae: A phylogenetic analysis. Evolution 42, 293–305 (1988).PubMed 
    Article 

    Google Scholar 
    115.Gagliardo, A. & Guilford, T. Why do warning-coloured prey live gregariously?. Proc. R. Soc. Lond. B Biol. Sci. 251, 69–74 (1993).ADS 
    Article 

    Google Scholar 
    116.Alatalo, R. V. & Mappes, J. Tracking the evolution of warning signals. Nature 382, 708–710 (1996).ADS 
    CAS 
    Article 

    Google Scholar 
    117.Yachi, S. & Higashi, M. The evolution of warning signals. Nature 394, 882–884 (1998).ADS 
    CAS 
    Article 

    Google Scholar 
    118.Lindström, L., Alatalo, R. V., Mappes, J., Riipi, M. & Vertainen, L. Can aposematic signals evolve by gradual change?. Nature 397, 249–251 (1999).ADS 
    Article 

    Google Scholar 
    119.Guilford, T., Nicol, C., Rotschild, M. & Moore, B. P. The biological roles of pyrazines: Evidence for a warning odour function. Biol. J. Linn. Soc. 31, 113–128 (1987).Article 

    Google Scholar 
    120.Arenas, L. M., Walter, D. & Stevens, M. Signal honesty and predation risk among a closely related group of aposematic species. Sci. Rep. 5, 11021. https://doi.org/10.1038/srep11021 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    121.Hämäläinen, L., Mappes, J., Rowland, H. M., Teichmann, M. & Thorogood, R. Social learning within and across predator species reduces attacks on novel aposematic prey. J. Anim. Ecol. 89, 1153–1164 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    122.Landova, E., Hotova Svadova, K., Fuchs, R., Stys, P. & Exnerova, A. The effect of social learning on avoidance of aposematic prey in juvenile great tits (Parus major). Anim. Cogn. 20, 855–866 (2017).PubMed 
    Article 

    Google Scholar 
    123.Leimar, O. & Tuomi, J. Synergistic selection and graded traits. Evol. Ecol. 12, 59–71 (1998).Article 

    Google Scholar 
    124.Gompert, Z., Willmott, K. R. & Elias, M. Heterogeneity in predator micro-habitat use and the maintenance of Müllerian mimetic diversity. J. Theor. Biol. 281, 39–46 (2011).PubMed 
    Article 

    Google Scholar 
    125.Willmott, K. R., Willmott, J. C. R., Elias, M. & Jiggins, C. D. Maintaining mimicry diversity: Optimal warning colour patterns differ among microhabitats in Amazonian clearwing butterflies. Proc. R. Soc. B Biol. Sci. 284, 20170744 (2017).Article 

    Google Scholar 
    126.Van Belleghem, S. M., Roman, P. A. A., Gutierrez, H. C., Counterman, B. A. & Papa, R. Perfect mimicry between Heliconius butterflies is constrained by genetics and development. Proc. R. Soc. B Biol. Sci. 287, 20201267 (2020).Article 
    CAS 

    Google Scholar 
    127.Bocek, M. & Bocak, L. Species limits in polymorphic mimetic Eniclases net-winged beetles from New Guinean mountains (Coleoptera, Lycidae). Zookeys 593, 15–35 (2016).Article 

    Google Scholar 
    128.Do Nascimento, E. A. & Bocakova, M. A revision of the Neotropical genus Eurrhacus (Coleoptera: Lycidae). Ann. Zool. 67, 689–697 (2017).Article 

    Google Scholar  More