Development of the European Ladybirds Smartphone Application: A Tool for Citizen Science

Introduction

Citizen science, otherwise known as public participation in scientific research or community science, can be a powerful tool to obtain data on insect diversity and abundance across larger spatial scales whilst simultaneously promoting education and awareness about insects (e.g., Eitzel et al., 2017; Gardiner and Roy, 2021). Indeed, considering reports of global insect declines (e.g., Hallmann et al., 2017; Cardoso and Leather, 2019; Wagner et al., 2021), enhancing citizen science or community science, especially in areas where academic or professional infrastructure is lacking, was one of the immediate actions proposed by scientists when formulating a roadmap for insect conservation and recovery (Harvey et al., 2020). Cardoso et al. (2011) recognized the role of citizen science as part of the solution for the scarce and underfunded science on invertebrates, including the declining number of insect taxonomists. There are various typologies of citizen science and viewpoints on what is or is not citizen science (Haklay et al., 2021). Here, we focus on volunteers and their contributions to field-based observations in a coordinated effort involving professional scientists (Bonney, 1996).

Ladybirds (Coleoptera: Coccinellidae) are popular and charismatic insects. More than 6,000–7,000 species have been described worldwide (Seago et al., 2011). The brightly colored forewing patterns of ladybirds enable relatively easy identification to species-level from photographs for most species (e.g., Jouveau et al., 2018). As such, ladybirds from the more conspicuous groups (Coccinellinae, Epilachninae, Chilocorinae) are highly suitable for engaging people within citizen science projects (e.g., Gardiner et al., 2012).

Ladybirds are very diverse in terms of biology and ecology. Different species can be found in many terrestrial habitats (e.g., deciduous and coniferous forest, meadows and marshes, heathlands, croplands) where they exploit a range of prey species (e.g., aphids, coccids, whiteflies, mites, fungi) (for more detail, see Hodek et al., 2012). Some species display specific life history traits such as habitat and/or dietary specialization, myrmecophily and aggregation behavior which make them attractive to naturalists and fascinating to the public (Adriaens et al., 2015a). Although ladybirds are considered one of the most well-studied groups of insects, there are many knowledge gaps and scientific discoveries still to be made about them. Recently there was a first report of parthenogenesis in ladybirds (Magro et al., 2020); a group that, until recently, was considered to have only sexual reproduction.

While Jarić et al. (2020) reported that the charisma of a species (sensu Ducarme et al., 2013) highly affects the public’s approach toward it, Groom et al. (2021) suggest that the target species/group needs to also evoke emotion or connection in the participants and that this is probably more important than simply the degree to which the species is considered charismatic. It is known that in zoo gardens, an animal’s beauty and (large) size are generally more important to visitors than is conservation status (Frynta et al., 2013). In citizen science the connection to volunteers (i.e., citizens, scientists, biodiversity managers, policy-makers, local authorities, industry, schools, and other participants) can be positively (e.g., Sequeira et al., 2014) or negatively emotive (e.g., Gallo and Waitt, 2011; Palmer et al., 2017; Porter et al., 2019). European ladybirds are deeply rooted in popular culture and are undoubtedly regarded as both emotive and charismatic. They may invoke positive or negative emotions (e.g., Shipley and Bixler, 2017). As an example, the arrival of the invasive alien harlequin ladybird, Harmonia axyridis (Pallas) has been the motivation for increasing participation in established ladybird recording schemes worldwide (e.g., Roy and Brown, 2015; Grez et al., 2016; Hiller and Haelewaters, 2019). This species was introduced to many countries, has spread rapidly across the globe and is considered a threat to native biodiversity (Roy et al., 2012, 2016). Harmonia axyridis is regarded both positively, for being charismatic and for the ecosystem services it provides (Riddick, 2017), and negatively, adversely affecting other species of aphid natural enemy through competition and intra-guild predation (Roy et al., 2012; Brown et al., 2015a; Kenis et al., 2017; Masetti et al., 2018; Zaviezo et al., 2019). Additionally it is considered a nuisance to humans in some contexts.

Mobile applications (apps) have played a key role in facilitating the participation of volunteers in citizen science projects (August et al., 2015; Chandler et al., 2017). Mobile apps can help record the location of a species and allow for fast and easy submission of records without data loss when connectivity is good (Teacher et al., 2013). Nowadays, there are numerous mobile apps available for biological recording, with a general or specific taxonomic scope, and some with advanced built-in image recognition tools to facilitate species identification (e.g., iNaturalist, Observation.org or Pl@ntNet). Most Europe-wide biodiversity projects capture occurrence information (opportunistic data) to support atlas projects (e.g., butterflies—Settele et al., 2008; birds—Herrando et al., 2019; mammals—Mitchell-Jones et al., 1999), and increasingly use records collected via citizen science initiatives using mobile apps. Recent statistical developments provide methods for assessing biodiversity trends and indicators (e.g., Termaat et al., 2019) at large scales, using opportunistic data collected through citizen science (Isaac et al., 2014). Structured, abundance sampling schemes and partnerships also provide biodiversity assessments at the European scale. Schemes for butterflies are the most established for insects and provide European indicators for measuring progress toward biodiversity targets (e.g., Sustainable Development Goal: Life on Land; van Swaay et al., 2019). It is widely recognized that there is potential to increase the contribution of citizen science to enhance our understanding of trends across many insect groups (Gardiner and Roy, 2021).

Here, we provide an overview, including the rationale, of the development of a dedicated mobile app for European ladybird identification and recording. Our main aims in designing the application were to engage diverse audiences in sharing their sightings of ladybirds whilst providing information on ladybird ecology and identification to participants, in order to improve appreciation of the diversity and value of these popular beetles. We provide technical specifications of the application, including mechanisms for data sharing, data quality and record validation. Finally, we outline potential approaches for using this recording tool to enhance trans-national collaboration on ladybird mapping in Europe.

Monitoring of European Ladybirds in Seminal National Projects

Various European countries have operated ladybird recording schemes of different kinds for several decades. Some of the schemes are run at a national level whilst others are regional. Such schemes, as detailed below, were key in developing the ideas for a pan-European approach to ladybird recording.

United Kingdom

There has been a national recording scheme for ladybirds in the United Kingdom since 1971. This evolved into the United Kingdom Ladybird Survey¹ in 2005, one of the first online wildlife recording schemes (Brown et al., 2008). Together these have engaged tens of thousands of people with recording the distribution and ecology of ladybirds in the United Kingdom, contributing over 229,000 verified records. The United Kingdom Ladybird Survey launched the smartphone app iRecord Ladybirds in 2013. The current European Ladybird App builds on that model. The substantial recording effort in the United Kingdom has greatly increased our understanding of the distribution and ecology of native and introduced ladybird species. In particular, verified records of H. axyridis have allowed the unusual opportunity of highly detailed mapping of the spread of a new invasive species (Brown et al., 2008, 2018).

Czech Republic

Monitoring of ladybirds in the Czech Republic has been partially covered by the work of the Nature Conservation Agency of the Czech Republic (AOPK CR), which monitors all living organisms using the BioLog and iNaturalist applications. There is also monitoring of H. axyridis on the popular BioLib server. In 2019, the NAJDI.JE² platform was launched for monitoring invasive invertebrates in the Czech Republic using citizen science, including H. axyridis overwintering sites. Additionally the databases of taxonomists Ivo Kovář and Oldřich Nedvěd contain a large amount of data, obtained by determining records for a very large base of amateur entomologists within the Czech Entomological Society.

No targeted ladybird monitoring project has yet been created in the Czech Republic, so the European Ladybird App will enable widespread recording of ladybirds in the country.

Belgium

In Belgium, a large-scale citizen science ladybird mapping project was launched in 1999. Skilled volunteer recorders collected standardized data on ladybird occurrence and ecology using a standard recording form (Adriaens et al., 2008). The aim was to use these data to publish distribution atlases (Branquart et al., 1999; Adriaens and Maes, 2004) and a Red List (Adriaens et al., 2015a). The project was supported by the Research Centre for Nature, Forests and Wood in the Walloon Region and the Institute for Nature Conservation (INBO) in Flanders. Observations were underpinned with pictures or other means of verification (e.g., based on recorder experience). Updated distribution maps were published regularly and people were actively stimulated to fill gaps through dedicated searches in insufficiently sampled grid squares. The project engaged about 800 volunteers actively submitting records. The data gathered were openly published on the Global Biodiversity Information Facility in 2012 (Adriaens et al., 2021). Since 2008, after the launch of the online reporting portal³ and its mobile phone applications by the conservation NGO Natuurpunt (cf. Swinnen et al., 2018), paper recording was replaced by online recording which greatly increased the number of ladybird observations, the speed of record submission, the number of volunteers as well as the spatial resolution and quality of ladybird records. As this platform is well established for recording, the European Ladybird App is anticipated to be used less used in Belgium by the established naturalist community, though it might still appeal to people wanting to increase their ladybird identification skills, wanting to contribute to European ladybird mapping specifically, as well as to a crowd outside the classical recording community. As several recording tools generate useful ladybird data, the focus should be on openly publishing data and sharing them through the application of data standards and interoperability (Adriaens et al., 2015b; Groom et al., 2016).

Slovakia

Haviar (2007) contributed much to the knowledge of occurrence, distribution and ecology of ladybirds in Slovakia. Related short-term monitoring and research activities in this country targeted communities of arboricolous ladybirds in forest and urban habitats (Panigaj et al., 2014; Viglášová et al., 2017; Holecová et al., 2018) and the year-round dynamics of H. axyridis in Scots pine forest habitats (Zach et al., 2020). The citizen science project Ladybirds of Slovakia (2015–2017)⁴ focused on ladybird data collection from volunteers via Facebook.

Portugal

In the Azores (Portugal), since 2019, a project that allows citizens to assist in the monitoring of ladybirds is available.⁵ Under this project, face-to-face activities are organized for schools of all levels of education and institutions with children in need. Scientists and students undertake field work and training to collect and record ladybirds. Under this project, two important outputs were already produced; an updated checklist of the ladybird species of Portugal, including the Azores and Madeira archipelagos (Soares et al., 2021) and a biodiversity database of ladybirds (Coleoptera: Coccinellidae) of the Azores archipelago (in prep.). There is no equivalent project for mainland Portugal, so the European Ladybird App will enable widespread recording of ladybirds in the country.

Italy

Many short-term monitoring and research activities informed the knowledge of habitats and distribution of ladybirds in Italy. Many local papers updated the distribution of Harmonia axyridis at regional level and data from citizen science, i.e., iNaturalist or local bioblitzes (see Menchetti et al., 2016), have been used in scientific literature. There is no global recording scheme for ladybirds in Italy, so the European Ladybird App will enable widespread recording of ladybirds in the country (Figure 1).

FIGURE 1

Figure 1. Screenshots from the European Ladybirds smartphone application (app) used to record ladybird species, with Adalia bipunctata used as an example throughout. Records submitted are checked iRecord: (A) opening screen; (B) ladybird guide: providing identification information for the species selected, in this case Adalia bipunctata; (C) ladybird guide: first screen, showing a list of species available to record, ranked by likelihood of occurrence; (D) ladybird guide: first screen, showing a list of species available to record, filtered by four traits of the ladybird; (E) adding a record: main recording screen once a species has been selected; (F) information: screen provides background information about the app; (G) information: screen provides for language selection; (H) information: screen provides for country selection.

Collaboratively Developing the European Database of Ladybirds

In developing this application we first set up a team with expertise in coccinellids from six countries (United Kingdom, Czech Republic, Slovakia, Italy, Belgium, and Portugal) (Figure 1). We collaboratively prepared a database of ladybird species established within each country. We excluded small, so-called inconspicuous ladybird species, which are known to be difficult to identify (e.g., the genus Scymnus). Currently, 72 taxa are documented in the database, including various color forms for some species (e.g., H. axyridis has six color forms across the countries) (Figure 1C). For each species, we included the following information to support identification (Figure 1B): (1) morphology (size, elytral coloration, pattern on pronotum, presence of melanic forms, information about spot fusions, coloration of legs, number of spots), (2) ecology (prey, habitat, plants and overwintering habitat), and (3) three photos of adults (where available). To maximize accessibility to volunteers across the participating countries, we translated all the text into the official languages for each country.

Technical Specifications

This open-source mobile application (link)⁶ was developed using standard web-based technologies (HTML, CSS, JavaScript). This way we were able to reuse many supporting open-source libraries and tools which helped to streamline the development process. The app is essentially a responsive website that is designed to work well on small mobile devices. As a website it couldn’t be directly installed onto users’ smartphone devices therefore it was wrapped with a Cordova container. Traditionally, mobile applications are re-written for each mobile platform but packaging the code in such a way allows reuse of the same codebase for multiple platforms. Such an app is called a Hybrid and it can be deployed to both iOS and Android app stores.

The app has species names and other related content translated and managed by multiple collaborators from different countries (Figure 1G). The species datasheet is extensive and currently holds over 160 columns with species-related information. We are hosting the datasheet online on OneDrive cloud which essentially is our simple but flexible real-time content management system. We have agreed on a custom column header formatting schema which allowed us to write a command-line script to transform the columns into a JSON-formatted file which is then pulled into the app programmatically. In such a way, collaborators from multiple countries can update the content in parallel and the updates can then be imported into the app with little effort and few errors.

Using a Microsoft Excel spreadsheet for translations for multiple countries wasn’t very practical, so we use the Transifex web platform for managing species and app interface translations. At the time of writing, it is free for open-source projects such as this and allows us to pull the translations into the app.

The app is linked to an open-source Indicia database (warehouse)⁷ where the records are stored. It has a lot of tooling to streamline the verification process and to export and exchange data with other systems. Indicia has extensive online documentation⁸ of all aspects of installing and maintaining a data warehouse to support data capture projects, including mobile application approaches such as European Ladybird App (Figure 1). The system architecture, data model and coding conventions allow any developers to contribute to the open source development of the software through the project Github repository.⁹

Data Quality and Validation

The use of Indicia for data storage gives a flexible solution for data sharing agreements and allowing species records to be linked to the same user accounts from multiple connected mobile applications and websites. One of the sites our mobile app is linked to is iRecord¹⁰ which is used in the United Kingdom for sharing wildlife observations, supports multiple recording apps such as this and has a big community of recorders and verifiers.

iRecord incorporates verification rules developed by national recording schemes for a desktop application (the National Biodiversity Network Record Cleaner). Validation is assisted by automated record checks which highlight records outside the known spatial or temporal range of the species, and records of species which are difficult to identify. If records are highlighted by Record Cleaner the observer receives a message, with the option of editing the record. The expert verification of records on iRecord applies a two tier approach. Verifiers choose from a set of validation categories that they can apply to a record. A record is accepted as meeting the standard required for inclusion by the recording scheme or project in question when a verifier accepts it as correct on the basis of the submitted photo or is considered correct when the verifier has not seen photo/s or specimen/s (or cannot be absolutely sure of the identification from submitted photo/s) but has a high degree of confidence that the record is likely to be correct, based on difficulty of ID, date, location and recorder skills/experience etc. Other categories include unable to verify, incorrect, unconfirmed or plausible.

Citizen Focus

The application requires participants to create a record of the ladybird they observe and so, it is necessary for them to identify the species, which will later be verified by an expert. Additionally, the following information is requested: the coordinates of the location (usually derived from mobile phone GPS), date, number of individuals, habitat where the individual was found, and a photo (to enable identification). To increase the ease of use we selected the three most specific morphological features (main color, size, and pronotum pattern) and coupled these with country-based ranking of the relative occurrence (based on the total number of grid cells with observations of the species) for each species. Such filters (Figure 1D) enable the users to select from a reduced number of likely species when recording, thus helping to reduce misidentifications.

Potential Use of Data

Information collated through the European Ladybird App will be openly available to address many potential questions but we focus on three main areas: (1) Understanding the ecology and distribution of ladybird species; (2) Informing ladybird conservation; (3) Education and engagement in biological recording and entomology. In a preliminary release of the European Ladybird App, we received over 1,600 records of 26 species between January 2019 and May 2021, mostly from GB and Ireland but also from other places in Europe. About 75% of these records have been accepted as accurate, indicating the high potential of this app for citizen science.

This initiative is the first step of a collaborative approach involving the recording of ladybirds through citizen science across Europe¹¹ (Supplementary Figure 1). Currently, the application builds on existing collaborations between six countries that have ladybird recording, but in the long-term we aim to include additional countries and use the data generated to produce a European ladybird distribution atlas. This will also require integrating the data from the ladybird app with other available data on ladybird distribution. This can be achieved through an open approach to publishing and sharing data from the app and the promotion of the app with other active mapping projects in Europe. Long-term conservation trends for ladybirds are so far only available for very limited regions (e.g., United Kingdom; Roy and Brown, 2018) or databases (e.g., GBIF—the Global Biodiversity Information Facility) and we aim to use the European data to inform Red List assessments (Maes et al., 2015)¹² Additionally the app has the potential to generate timely data on the arrival of new ladybird species in a country: for example in the United Kingdom, the first records of Oenopia conglobata L. were received via similar citizen science tools (Brown et al., 2015b).

Furthermore, ladybirds offer an appealing way of encouraging people to have an interest in entomology; in many ways ladybirds represent an “easy way in” to entomology, which can appear a daunting field. We consider the successful engagement of people to be as important as the ecology and conservation knowledge gained from the records themselves. The engagement benefits come from encouraging an interest in wildlife and the environment, as well as encouraging the next generation of entomologists and biological recorders. Additionally, connecting with nature is known to enhance the well-being of participants (Pritchard et al., 2020).

Conclusion

In conclusion, the development of the European Ladybird App highlights the value of collaborative partnerships in citizen science. By working on a shared platform and using infrastructures employed for other similar, but national initiatives, we have been able to cost-effectively develop an approach for people across Europe to engage with studying and recording ladybirds. Future work could focus on how the app is performing in different countries, which species are reported, recording biases etc. and how it can be improved to suit the needs of the recording community. There is an urgent need to gather evidence on the status and trends of insects over large spatial scales to inform conservation action going forward. Providing resources, such as this smartphone application, will play an important part in maximizing the potential of citizen science and increasing access and participation in the field of entomology.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

Author Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

Funding

JS, AH, and ZM were supported by the program VES19 INTER-COST No. MSMT-15739/2019-6 (MŠMT ČR); HR and DR by the Natural Environment Research Council award number NE/R016429/1 as part of the UK-SCAPE Programme delivering National Capability; PZ, SV, and JK by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic (grant VEGA 2/0032/19). All the authors acknowledge support from the Alien CSI COST Action Network CA17122 funded by the Horizon 2020 Framework Programme of the European Union. AOS was supported by FEDER in 85% and by Azorean Public funds by 15% through Operational Program Azores 2020, under the following project AZORESBIOPORTAL –PORBIOTA (ACORES-01-0145-FEDER-000072). Further funding for app development was provided by Anglia Ruskin University.

Conflict of Interest

KK was employed in UK Centre Hydrology and Ecology in Wallingford, United Kingdom, when this work was done. He was now an owner of Flumens Ltd.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.741854/full#supplementary-material

Footnotes

1. ^ https://www.coleoptera.org.uk/coccinellidae/home/
2. ^ https://www.najdije.cz
3. ^ www.waarnemingen.be
4. ^ https://www.facebook.com/lienkyslovenska
5. ^ www.joaninhasdosacores.com
6. ^ https://github.com/NERC-CEH/leu-app
7. ^ http://www.indicia.org.uk/
8. ^ https://indicia-docs.readthedocs.io/en/latest/index.html
9. ^ https://github.com/Indicia-Team/
10. ^ https://www.brc.ac.uk/irecord/
11. ^ https://european-ladybirds.brc.ac.uk/home
12. ^ https://www.iucn.org/commissions/ssc-groups/invertebrates/ladybird

References

Adriaens, T., Gomez, G., and Maes, D. (2008). Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. BioControl 53, 69–88. doi: 10.1007/s10526-007-9137-6

CrossRef Full Text | Google Scholar

Adriaens, T., and Maes, D. (2004). Voorlopige verspreidingsatlas van lieveheersbeestjes in vlaanderen, resultaten van het lieveheersbeestjesproject van de jeugdbonden. Bertram 2, 1–69.

Google Scholar

Adriaens, T., San Martin y Gomez, G., Bogaert, J., Crevecoeur, L., Beuckx, J. P., and Maes, D. (2015a). Testing the applicability of regional IUCN Red List criteria on ladybirds (Coleoptera, Coccinellidae) in Flanders (north Belgium): opportunities for conservation. Insect Conserv. Divers. 8, 404–417. doi: 10.1111/icad.12124

CrossRef Full Text | Google Scholar

Adriaens, T., Sutton-Croft, M., Owen, K., Brosens, D., van Valkenburg, J., Kilbey, D., et al. (2015b). Trying to engage the crowd in recording invasive alien species in Europe: experiences from two smartphone applications in northwest Europe. Manag. Biol. Invasions 6, 215–225. doi: 10.3391/mbi.2015.6.2.12

CrossRef Full Text | Google Scholar

Adriaens, T., San Martin y Gomez, G., Maes, D., Brosens, D., and Desmet, P. (2021). Belgian Coccinellidae - Ladybird beetles in Belgium. Version 1.4. Brussels: Research Institute for Nature and Forest (INBO).

Google Scholar

August, T., Harvey, M., Lightfoot, P., Kilbey, D., Papadopoulos, T., and Jepson, P. (2015). Emerging technologies for biological recording. Biol. J. Linn. Soc. 115, 731–749. doi: 10.1111/bij.12534

CrossRef Full Text | Google Scholar

Bonney, R. (1996). Citizen science: a lab tradition. Living Bird 15, 7–15.

Google Scholar

Branquart, E., Baugnée, J.-Y., Mairesse, J. L., and Gaspar, C. (1999). Inventaire de la Faune des Coccinelles de Wallonie (Chilocorinae, Coccinellinae et Epilachninae). Rapport final. Gembloux: Faculté universitaire des Sciences agronomiques.

Google Scholar

Brown, P. M. J., Harrower, C., Dean, H. J., Rorke, S. L., and Roy, H. E. (2018). Spread of a model invasive alien species - the harlequin ladybird Harmonia axyridis in Britain and Ireland. Sci. Data 5:180239. doi: 10.1038/sdata.2018.239

PubMed Abstract | CrossRef Full Text | Google Scholar

Brown, P. M. J., Ingels, B., Wheatley, A., Rhule, E. L., De Clercq, P., Van Leeuwen, T., et al. (2015a). Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomol. Sci. 18, 130–133. doi: 10.1111/ens.12092

CrossRef Full Text | Google Scholar

Brown, P. M. J., Roy, H. E., and Comont, R. (2015b). Wildlife reports: ladybirds. Br. Wildl. 26, 285–287.

Google Scholar

Brown, P. M. J., Roy, H. E., Rothery, P., Roy, D. B., Ware, R. L., and Majerus, M. E. (2008). Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl 53, 55–67. doi: 10.1007/s10526-007-9124-y

CrossRef Full Text | Google Scholar

Cardoso, P., Erwin, T. L., Borges, P. A. V., and New, T. R. (2011). The seven impediments in invertebrate conservation and how to overcome them. Biol. Conserv. 144, 2647–2655. doi: 10.1016/j.biocon.2011.07.024

CrossRef Full Text | Google Scholar

Cardoso, P., and Leather, S. R. (2019). Predicting a global insect apocalypse. Insect Conserv. Divers. 12, 263–267. doi: 10.1111/icad.12367

CrossRef Full Text | Google Scholar

Chandler, M., See, L., Copas, K., Bonde, A. M., López, B. C., Danielsen, F., et al. (2017). Contribution of citizen science towards international biodiversity monitoring. Biol. Conserv. 213, 280–294. doi: 10.1016/j.biocon.2016.09.004

CrossRef Full Text | Google Scholar

Ducarme, F., Luque, G. M., and Courchamp, F. (2013). What are “charismatic species” for conservation biologists. BioSci. Master Rev. 10, 1–8.

Google Scholar

Eitzel, M. V., Cappadonna, J. L., Santos-Lang, C., Duerr, R. E., Virapongse, A., West, S. E., et al. (2017). Citizen science terminology matters: exploring key terms. Citiz. Sci. 2:1. doi: 10.5334/cstp.96

CrossRef Full Text | Google Scholar

Frynta, D., Šimková, O., Lišková, A., and Landová, E. (2013). Mammalian collection on noah’s ark: the effects of beauty, brain and body size. PLoS One 8:e63110. doi: 10.1371/journal.pone.0063110

PubMed Abstract | CrossRef Full Text | Google Scholar

Gallo, T., and Waitt, D. (2011). Creating a successful citizen science model to detect and report invasive species. BioScience 61, 459–465. doi: 10.1525/bio.2011.61.6.8

CrossRef Full Text | Google Scholar

Gardiner, M. M., Allee, L. L., Brown, P. M. J., Losey, J. E., Roy, H. E., and Smyth, R. R. (2012). Lessons from lady beetles: accuracy of monitoring data from US and UK citizen-science programs. Front. Ecol. Environ. 10, 471–476. doi: 10.1890/110185

CrossRef Full Text | Google Scholar

Gardiner, M. M., and Roy, H. E. (2021). Community science and entomology. Annu. Rev. Entomol. doi: 10.1146/annurev-ento-072121-075258 [Epub ahead of print].

CrossRef Full Text | PubMed Abstract | Google Scholar

Grez, A., Zaviezo, T., Roy, H. E., Brown, P. M. J., and Bizama, G. (2016). Rapid spread of Harmonia axyridis in Chile and its effects on local coccinellid biodiversity. Diver. Distrib. 22, 982–994. doi: 10.1111/ddi.12455

CrossRef Full Text | Google Scholar

Groom, Q., Pernat, N., Adriaens, T., de Groot, M., Jelaska, S. D., Marèiulynienë, D., et al. (2021). Species interactions: Next level citizen science. Ecography. doi: 10.1111/ecog.05790 [Epub ahead of print].

CrossRef Full Text | Google Scholar

Groom, Q., Weatherdon, L., and Geijzendorffer, I. R. (2016). Is citizen science an open science in the case of biodiversity observations? J. Appl. Ecol. 54, 612–617. doi: 10.1111/1365-2664.12767

CrossRef Full Text | Google Scholar

Haklay, M., Fraisl, D., Tzovaras, B. G., Hecker, S., Gold, M., Hager, G., et al. (2021). Contours of citizen science: a vignette study. R. Soc. Open Sci. 8:202108. doi: 10.1098/rsos.202108

PubMed Abstract | CrossRef Full Text | Google Scholar

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., et al. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12:e0185809. doi: 10.1371/journal.pone.0185809

PubMed Abstract | CrossRef Full Text | Google Scholar

Harvey, J. A., Heinen, R., Klein, A.-M., Armbrecht, I., Basset, Y., Baxter-Gilbert, J. H., et al. (2020). International scientists formulate a roadmap for insect conservation and recovery. Nat. Ecol. Evol. 4, 174–176. doi: 10.1038/s41559-019-1079-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Haviar, M. (2007). Biodiversity of Ladybirds of Slovakia (Coleoptera: Coccinellidae): Species Richness, Distribution, Hypsometry, Zoogeography, Ecology. Ph.D. thesis. (Bratislava: Comenius University in Bratislava), 125.

Google Scholar

Herrando, S., Keller, V., Bauer, H. G., Brotons, L., Eaton, M., Kalyakin, M., et al. (2019). Using the first European Breeding Bird Atlas for science and perspectives for the new Atlas. Bird Study 66, 149–158.

Google Scholar

Hiller, T., and Haelewaters, D. (2019). A case of silent invasion: citizen science confirms the presence of Harmonia axyridis (Coleoptera, Coccinellidae) in Central America. PLoS One 14:e0220082. doi: 10.1371/journal.pone.0220082

PubMed Abstract | CrossRef Full Text | Google Scholar

Hodek, I., van Emden, H. F., and Honek, A. (2012). Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Chichester: Wiley-Blackwell.

Google Scholar

Holecová, M., Zach, P., Hollá, K., Šebestová, M., Klesniaková, M., Šestáková, A., et al. (2018). Overwintering of ladybirds (Coleoptera: Coccinellidae) on Scots pine in Central Europe. Eur. J. Entomol. 115, 658–667. doi: 10.14411/eje.2018.065

CrossRef Full Text | Google Scholar

Isaac, N. J. B., van strien, A. J., August, T. A., de Zeeuw, M. P., and Roy, D. B. (2014). Statistics for citizen science: extracting signals of change from noisy ecological data. Methods Ecol. Evol. 5, 1052–1060. doi: 10.1111/2041-210X.12254

CrossRef Full Text | Google Scholar

Jarić, I., Courchamp, F., Correia, R. A., Crowley, S. L., Essl, F., Fischer, A., et al. (2020). The role of species charisma in biological invasions. Front. Ecol. Environ. 18, 345–353. doi: 10.1002/fee.2195

CrossRef Full Text | Google Scholar

Jouveau, S., Delaunay, M., Vignes-Lebbe, R., and Nattier, R. (2018). A multi-access identification key based on colour patterns in ladybirds (Coleoptera, Coccinellidae). ZooKeys 758, 55–73. doi: 10.3897/zookeys.758.22171

PubMed Abstract | CrossRef Full Text | Google Scholar

Kenis, M., Adriaens, T., Brown, P. M. J., Katsanis, A., San Martin, G., Branquart, E., et al. (2017). Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study. BioControl 62, 341–354. doi: 10.1007/s10526-016-9764-x

CrossRef Full Text | Google Scholar

Maes, D., Isaac, N. J., Harrower, C. A., Collen, B., Van Strien, A. J., and Roy, D. B. (2015). The use of opportunistic data for IUCN Red List assessments. Biol. J. Linn. Soc. 115, 690–706. doi: 10.1111/bij.12530

CrossRef Full Text | Google Scholar

Magro, A., Lecompte, E., Hemptinne, J.-L., Soares, A. O., Dutrillaux, A.-M., Murienne, J., et al. (2020). First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction. J. Zoolog. Syst. Evol. Res. 58, 194–208. doi: 10.1111/jzs.12339

CrossRef Full Text | Google Scholar

Masetti, A., Magagnoli, S., Lami, F., Lanzoni, A., and Burgio, G. (2018). Long term changes in the communities of native ladybirds in Northern Italy: impact of the invasive species Harmonia axyridis (Pallas). BioControl 63, 665–675. doi: 10.1007/s10526-018-9891-7

CrossRef Full Text | Google Scholar

Menchetti, M., Mori, E., Ceccolioni, F., Paggetti, E., Pizzocaro, L., and Cianferoni, F. (2016). New occurrences of the alien invasive species Harmonia axyridis (Pallas, 1773) in Southern Italy (Coleoptera: Coccinellidae). Onychium 12, 137–139.

Google Scholar

Mitchell-Jones, A. J., Amori, G., Bogdanowicz, W., Krystufek, B., Reijnders, P. J. H., Spitzenberger, F., et al. (1999). The Atlas of European Mammals, Vol. 3. London: Academic Press.

Google Scholar

Palmer, J. R. B., Oltra, A., Collantes, F., Delgado, J. A., Lucientes, J., Delacour, S., et al. (2017). Citizen science provides a reliable and scalable tool to track disease-carrying mosquitoes. Nat. Commun. 8:916. doi: 10.1038/s41467-017-00914-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Panigaj, L’., Zach, P., Honek, A., Nedvěd, O., Kulfan, J., Martinkova, Z., et al. (2014). The invasion history, distribution and colour pattern forms of the harlequin ladybird beetle Harmonia axyridis (Coleoptera, Coccinellidae) in Slovakia, Central Europe. ZooKeys 412, 89–102. doi: 10.3897/zookeys.412.6587

PubMed Abstract | CrossRef Full Text | Google Scholar

Porter, W. T., Motyka, P. J., Wachara, J., Barrand, Z. A., Hmood, Z., McLaughlin, M., et al. (2019). Citizen science informs human-tick exposure in the Northeastern United States. Int. J. Health Geogr. 18:9. doi: 10.1186/s12942-019-0173-0

PubMed Abstract | CrossRef Full Text | Google Scholar

Pritchard, A., Richardson, M., Sheffield, D., and McEwan, K. (2020). The Relationship Between Nature Connectedness and Eudaimonic Well-Being: a meta-analysis. J. Happiness Stud. 21, 1145–1167. doi: 10.1007/s10902-019-00118-6

CrossRef Full Text | Google Scholar

Riddick, E. W. (2017). Spotlight on the positive effects of the ladybird Harmonia axyridis on agriculture. BioControl 62, 319–330. doi: 10.1007/s10526-016-9758-8

CrossRef Full Text | Google Scholar

Roy, H. E., Adriaens, T., Isaac, N. B., Kenis, M., San Martin y Gomez, G., Onkelinx, T., et al. (2012). Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18, 717–725. doi: 10.1111/j.1472-4642.2012.00883.x

CrossRef Full Text | Google Scholar

Roy, H. E., and Brown, P. M. J. (2015). Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecol. Entomol. 40, 336–348. doi: 10.1111/een.12203

PubMed Abstract | CrossRef Full Text | Google Scholar

Roy, H. E., and Brown, P. M. J. (2018). Field Guide to the Ladybirds of Britain and Ireland. Illustrated by Richard Lewington. London: Bloomsbury.

Google Scholar

Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., et al. (2016). The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18, 997–1044. doi: 10.1007/s10530-016-1077-6

CrossRef Full Text | Google Scholar

Seago, A. E., Giorgi, J. A., Li, J., and Slipinski, A. (2011). Phylogeny, classification and evolution of ladybird beetles (Coleoptera: Coccinellidae) based on simultaneous analysis of molecular and morphological data. Mol. Phylogenet. Evol. 60, 137–151. doi: 10.1016/j.ympev.2011.03.015

PubMed Abstract | CrossRef Full Text | Google Scholar

Sequeira, A. M., Roetman, P. E., Daniels, C. B., Baker, A. K., and Bradshaw, C. J. (2014). Distribution models for koalas in South Australia using citizen science-collected data. Ecol. Evol. 4, 2103–2114. doi: 10.1002/ece3.1094

PubMed Abstract | CrossRef Full Text | Google Scholar

Settele, J., Kudrna, O., Harpke, A., Kühn, I., Van Swaay, C., Verovnik, R., et al. (2008). Climatic Risk Atlas of European Butterflies. Sofia: Pensoft.

Google Scholar

Shipley, N. J., and Bixler, R. D. (2017). Beautiful bugs, bothersome bugs, and FUN bugs: examining human interactions with insects and other arthropods. Anthrozoös 30, 357–372.

Google Scholar

Soares, A. O., Calado, H. R., Franco, J. C., Aguiar, A. F., Andrade, M. M., Zina, V., et al. (2021). An annotated checklist of ladybeetle species (Coleoptera: Coccinellidae) of Portugal, including the Azores and Madeira Archipelagos. Zookeys 1053, 107–144. doi: 10.3897/zookeys.1053.64268

PubMed Abstract | CrossRef Full Text | Google Scholar

Swinnen, K., Vercayie, D., Vanreusel, W., Barendse, R., Boers, K., Bogaert, J., et al. (2018). Waarnemingen. be–Non-native plant and animal occurrences in Flanders and the Brussels Capital Region. Belgium. BioInvasions Rec. 7, 335–342. doi: 10.3391/bir.2018.7.3.17

CrossRef Full Text | Google Scholar

Teacher, A. G., Griffiths, D. J., Hodgson, D. J., and Inger, R. (2013). Smartphones in ecology and evolution: a guide for the app-rehensive. Ecol. Evol. 3, 5268–5278. doi: 10.1002/ece3.888

PubMed Abstract | CrossRef Full Text | Google Scholar

Termaat, T., van Strien, A. J., van Grunsven, R. H. A., De Knijf, G., Bjelke, U., Burbach, K., et al. (2019). Distribution trends of European dragonflies under climate change. Divers. Distrib. 25, 936–950. doi: 10.1111/ddi.12913

CrossRef Full Text | Google Scholar

van Swaay, C. A. M., Dennis, E. B., Schmucki, R., Sevilleja, C. G., Balalaikins, M., Botham, M., et al. (2019). The EU Butterfly Indicator for Grassland species: 1990-2017: Technical Report. Butterfly Conservation Europe & ABLE/eBMS. Available online at: www.butterfly-monitoring.net (accessed July 14, 2021).

Google Scholar

Viglášová, S., Nedvěd, O., Zach, P., Kulfan, J., Parák, M., Honek, A., et al. (2017). Species assemblages of ladybirds including the harlequin ladybird Harmonia axyridis: a comparison at large spatial scale in urban habitats. BioControl 62, 409–421. doi: 10.1007/s10526-017-9793-0

CrossRef Full Text | Google Scholar

Wagner, D. L., Grames, E. M., Forister, M. L., Berenbaum, M. R., and Stopak, D. (2021). Insect decline in the Anthropocene: death by a thousand cuts. Proc. Natl. Acad. Sci. U.S.A. 118, e2023989118. doi: 10.1073/pnas.2023989118

PubMed Abstract | CrossRef Full Text | Google Scholar

Zach, P., Holecová, M., Brabec, M., Hollá, K., Šebestová, K., Martinkova, Z., et al. (2020). Scots pine forest in Central Europe as a habitat for Harmonia axyridis: temporal and spatial patterns in the population of an alien ladybird. Folia Oecol. 47, 81–88. doi: 10.2478/foecol-2020-0010

CrossRef Full Text | Google Scholar

Zaviezo, T., Soares, A. O., and Grez, A. A. (2019). Interspecific exploitative competition between Harmonia axyridis and other coccinellids is stronger than intraspecific competition. Biol. Control 131, 62–68. doi: 10.1016/j.biocontrol.2018.12.008

CrossRef Full Text | Google Scholar