Citizen Science Reveals The Distribution of The Invasive
Citizen Science Reveals The Distribution of The Invasive
Citizen Science Reveals The Distribution of The Invasive
https://doi.org/10.1007/s10530-020-02312-7 (0123456789().,-volV)
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INVASION NOTE
Abstract The harlequin ladybird (Harmonia axyr- axyridis is widely distributed in Argentina but there
idis) was introduced in numerous countries around the are large gaps, particularly in arid regions. The
world as a biological control agent but nowadays it is invasion seems to be recent in the south of the country.
considered as a pest itself. It is a highly invasive Citizen science is a valuable tool for mapping invasive
species that has negative impacts on native biodiver- alien species in a large country like Argentina, and will
sity, may affect some crops, and causes a nuisance to help to monitor the continuous expansion of H.
humans. Despite its relevance worldwide, the invasion axyridis.
by H. axyridis in South America has received little
attention. Here we used a citizen science approach to Keywords Alien species Biological invasion
study the distribution of H. axyridis in Argentina Coccinellidae iNaturalist Pampa Patagonia
where the species was intentionally introduced in
1986. We also informally tested and evaluated the
preferences for different methods for reporting
records: iNaturalist website, Google form, email, Introduction
WhatsApp, and Facebook. Most records were reported
through WhatsApp and iNaturalist. We found that H. Invasive alien species are considered one of the major
drivers of biodiversity loss with serious impacts on not
Electronic supplementary material The online version of
only ecology but also economies and human health
this article (https://doi.org/10.1007/s10530-020-02312-7) con- (Dı́az et al. 2019). Harmonia axyridis (Pallas)
tains supplementary material, which is available to authorized (Coleoptera, Coccinellidae) is a highly invasive alien
users.
species that is widely distributed worldwide (Cama-
V. Werenkraut (&) F. Baudino cho-Cervantes et al. 2017; Roy et al. 2016). It is native
Laboratorio Ecotono, Centro Regional Universitario to Asia and has been introduced as a biological control
Bariloche, Universidad Nacional del Comahue/ agent in many countries and also accidentally in many
INIBIOMA-CONICET, Quintral 1250, 8400 Bariloche,
others. Nowadays it has established populations in at
Rio Negro, Argentina
e-mail: vicwkt@gmail.com least 59 countries outside its native range (Camacho-
Cervantes et al. 2017; Roy et al. 2016) and it is found
H. E. Roy on all continents except Australia and Antarctica. This
Centre for Ecology and Hydrology, Natural Environment
species has negative impacts on native biodiversity
Research Council, Maclean Building, Benson Lane,
Crowmarsh Gifford, Wallingford, (Brown and Roy 2018; Grez et al. 2016) and it might
Oxfordshire OX10 8BB, UK affect some crops and the wine industry (Ameixa et al.
123
V. Werenkraut et al.
2019; Koch and Galvan 2008). It usually causes a in 1986 (Garcı́a et al. 1999) and by 2001 it was
nuisance to humans by overwintering inside houses in detected around 1000 km away to the east (Buenos
large numbers, and some allergic reactions and bites Aires; Saini 2004). By early June 2018 (before we
have been reported (Roy et al. 2016). Today, there is widely promoted our project) the species was consid-
general consensus amongst the scientific community ered to be present only in a few localities from the
that the negative impacts of H. axyridis outweigh its centre of the country to * 39° S (Montero and
benefits as a biological control agent (Camacho- Vignaroli 2008; Olave 2016; Saini 2004; Fig. 1a,
Cervantes et al. 2017; Majerus et al. 2006). It is also Online Resource 2, Table 2a). Recently, Hiller and
regarded as a model species and as an opportunity for Haelewaters (2019) mapped the distribution of H.
global collaborations for the understanding of invasion axyridis in Central and South America using Flickr,
biology (Roy and Wajnberg 2008; Roy et al. 2016). iNaturalist, and museum records. For Argentina, they
The invasion of H. axyridis has been intensively found 24 records in Flickr (dated from 2006 to 2016)
studied in Europe and North America (e.g. Ameixa and 89 records in iNaturalist from which only 19 had
et al. 2019; Brown et al. 2008; Koch and Galvan been uploaded before the promotion of our project and
2008), but detailed analysis of the distribution of the only 15 represented independent points (four of them
species in most of the countries in South America is were duplicates). Taking these 43 records into
rather outdated or scarce (but see Grez et al. 2016; account, the registered distribution of H. axyridis in
Hiller and Haelewaters 2019). The species was Argentina by the end of May 2018, expanded
introduced as a biological control agent through the from * 27° S to * 39° S (Fig. 1a). Documenting
1980s and 1990s (Grez et al. 2016), and to date wild the distribution of H. axyridis in Argentina is the first
populations have been reported except in Bolivia, step to evaluating its impact on native species and the
French Guiana, Guyana and Suriname (Brown et al. economy and will also contribute to the general
2011; Camacho-Cervantes et al. 2017; Hiller and understanding of the ecology of this highly invasive
Haelewaters 2019; Montero and Vignaroli 2008; alien species.
Olave 2016 and see Online Resource 1 for more The study of the distribution of an insect in a large
details). However, the magnitude of its expansion in country using traditional techniques for biodiversity
the countries where it is present has only been studied surveys would be extremely expensive and time-
in Chile, where it shows a continuous distribution consuming. Citizen science is a powerful alternative to
from * 29° S to * 42° S, being absent only in the gather biodiversity data for wide geographical scales,
northern desert and in southern Patagonia (Grez et al. and it is also a way of engaging people with science,
2016). For Argentina, the similarity in climatic increasing their awareness of environmental issues
conditions and biomes with regions where H. axyridis (Dickinson et al. 2012). Today, the extensive use of
is native and climatic predictions suggest that almost email, internet and social networks provides an
the whole country is suitable for the establishment of unprecedented opportunity to reach people and
the species (Koch and Galvan 2008; Koch et al. 2006; receive information. In addition, engaging people in
Poutsma et al. 2007). recording ladybirds is promising since these insects
Argentina is a large country (* 2.7 million km2) are usually attractive to the public. Indeed, the
with a very diverse landscape. It extends * 33° in involvement of citizens in monitoring H. axyridis
latitude (extreme latitudes: 21° 460 S to 55° 030 S) has provided invaluable data in many countries (e.g.
and * 20° in longitude (extreme longitudes 53° 380 Grez et al. 2016; Purse et al. 2015; Veran et al. 2016).
W to 73° 340 W). It is mostly bordered by two strong Here, we used a citizen science approach to study the
barriers for the dispersal of many terrestrial species: distribution of H. axyridis in Argentina to test our
The Andes to the West and the Atlantic Ocean to the hypothesis that the species is widespread in the
East. It encompasses 14 biogeographic provinces country. In addition, we evaluated the preferences of
(excluding the Falkland Islands) from the subtropical Argentinean citizens in using different methods for
forests to the arid and cold Patagonian steppe (Arana reporting occurrences of this species.
et al. 2017), offering a wide range of conditions for the
establishment of invasive species. H. axyridis was
introduced into the Central-West region of Argentina
123
Citizen science reveals the distribution of the invasive harlequin ladybird
Fig. 1 Biogeographic regions in Argentina and the reported numbers in boxes indicate the year of the first reported
presence of H. axyridis: a before June 2018, and b after this establishment taken from literature (it does not include the year
study. a The arrow indicates the point of introduction and of pictures from iNaturalist and Flickr)
123
V. Werenkraut et al.
123
Citizen science reveals the distribution of the invasive harlequin ladybird
Distribution of H. axyridis in Argentina Argentina. Future genetic analysis might help track
the route of the invasion in the Valdivian Forest and
Taking this project and Ecoregistros records together, the Patagonian provinces.
H. axyridis in Argentina seems to extend from at least In Ecoregistros, we found an extreme record
24° to 43° S and from 71° 300 to 54° W, having arrived at * 48° S, 66° W in the west of the Patagonian
in ten biogeographical regions (Fig. 1b; Online province sent in 2017 (Puerto Deseado; Fig. 1b). We
Resource 3). The southern limit is mismatched with contacted the user who sent this record and it seems the
climatic predictions (Koch et al. 2006; Poutsma et al. species is not established in this locality as it has not
2007), but is climatically similar to some regions from been seen again. Our project began almost 20 years
which reports were generated in Chile (Alaniz et al. after the first signs of invasion of H. axyridis in
2018; Grez et al. 2016) and to high latitudes in the Argentina, and thus our citizen science records are not
United Kingdom, where the species shows limited suitable to track its invasion across the country as has
abundance in northern England and Scotland (Purse been done in other countries (e.g. Grez et al. 2016;
et al. 2015; Roy et al. 2016). This high latitude limit in Purse et al. 2015; Veran et al. 2016). Nonetheless, the
the invaded region has been related to the combination recent invasion in the Valdivian Forest and the
of low temperatures and high precipitation (Alaniz presence of the species in some localities in the
et al. 2018; Roy et al. 2016) and to the low density of adjacent Patagonian province indicate that our study is
urban areas (Purse et al. 2015). In our study, most of timely for monitoring the expansion and assessing the
the southern records were reported in the Valdivian impacts of H. axyridis in one of the most austral
Forest, close to the Andes, where precipitation is high regions of the world.
([ 2000 mm/year) compared to the east of the country Our study expands the range of H. axyridis * 600
(ca. 300 mm/year) (Barros et al. 1983). Although km further north than in Chile where the species seems
precipitation is high in the Valdivian Forest, these to be restricted due to the presence of the Atacama
records came mostly from or close to urban areas Desert (Alaniz et al. 2018; Grez et al. 2016). Never-
which might be promoting the invasion of the species. theless, our records in the north correspond to a small
Human-altered habitats, like towns and cities, promote region of subtropical forests in the East (Paraná Forest
biological invasions (Hufbauer et al. 2012) and have and Araucaria Forest) and West (Yungas) of Argen-
been mentioned as a factor shaping the invasion of H. tina, confirming the habitat matching predictions for
axyridis in particular (Grez et al. 2016; Purse et al. this biome (Koch et al. 2006). Contrary to climatic
2015; Veran et al. 2016). The low population density matching predictions (Koch et al. 2006; Poutsma et al.
in the Patagonian province and the decrease in 2007), the distribution shows a large gap in most of
temperature toward the south might explain at least northern Argentina in the warm, arid/semi-arid Chaco,
in part the low abundance of records there. and in the arid Puna (despite having reinforced the
According to the number of records and the survey in these regions). Although the absence of
comments from citizens, the establishment of the records does not necessarily mean the absence of the
species in the Valdivian Forest seems to be very recent species, H. axyridis is rarely found in arid and warm
(2017–2018; Online Resource 3). The citizens report- regions of the world (Grez et al. 2016; Roy et al. 2016).
ing records in this region claim the species had not It should be noted that we also received records of the
been seen before the summer of 2017, and most of species in several scattered locations in the Monte
them reported an extraordinary abundance of over- (annual precipitation: 80–250 mm, mean annual tem-
wintering individuals inside houses in the autumn perature: 13–17.5 °C; Cabrera 1971), which is within
2019. This region has connections through road traffic the Arid Diagonal of South America. However, here
with neighbouring localities in Chile where the species again, the records came mostly from urban areas or
was reported in 2015 (Grez et al. 2016), thus one from irrigated and/or cultivated zones which are
possibility is that the invasion in this region came from known to promote biological invasions (Hufbauer
Chile. Supporting this idea, a citizen who frequently et al. 2012) and might be facilitating the presence of
travels between Osorno (Chile) and Bariloche (Ar- the species.
gentina) reported that she used to see this ladybird The most populated area of the country was also the
among her belongings when she unpacked in one with the highest number of records of H. axyridis
123
V. Werenkraut et al.
(Pampean region; Online Resource 3). The Pampas are as part of the UK-SCAPE programme delivering National
mainly warm temperate grasslands (mean annual Capability.
temperature 13–17 °C; Cabrera 1971) with precipita-
tion throughout the year (annual precipitation:
References
600–1100 mm; Cabrera 1971) that represents suit-
able climatic conditions for the establishment of H. Alaniz A, Grez A, Zaviezo T (2018) Potential spatial interaction
axyridis (Koch et al. 2006; Poutsma et al. 2007). Also of the invasive species Harmonia axyridis (Pallas) with
this region concentrates more than 70% of the native and endemic Coccinellids. J Appl Entomol
cultivated areas in Argentina (INTA, National Agri- 142:513–524
Ameixa OM, Šipoš J, Burda M et al (2019) Factors influencing
cultural Technology Institute). The high number of the introduction and spread of Harmonia axyridis in the
records in this area might be an artefact of our Iberian Peninsula. Biol Invasions 21:323–331
sampling method as in citizen science there is bias in Arana MD, Martinez GA, Oggero AJ et al (2017) Map and
the number of records towards highly populated areas shapefile of the biogeographic provinces of Argentina.
Zootaxa 4341:420–422
(Dickinson et al. 2010). This might be the case, but the
Barros V, Cordon V, Moyano C et al (1983) Cartas de precip-
reported presence of the species since 2001 (Saini itación de la zona Oeste de las Provincias de Rı́o Negro y
2004), the highly invasive behaviour of H. axyridis Neuquén. Primera contribución. CONICET, Univ. Nacio-
(Roy and Wajnberg 2008), the wide distribution of nal del Comahue, Rı́o Negro
Brown PM, Roy HE (2018) Native ladybird decline caused by
records in this area, and the climatic suitability of this the invasive harlequin ladybird Harmonia axyridis: evi-
region (Koch et al. 2006; Poutsma et al. 2007), dence from a long-term field study. Insect Conserv Divers
reasonably suggest that the species is widely estab- 11:230–239
lished in the Pampas. Brown P, Adriaens T, Bathon H et al (2008) Harmonia axyridis
in Europe: spread and distribution of a non-native coc-
cinellid. Biocontrol 53:5–21
Citizen science as a powerful tool Brown PM, Thomas CE, Lombaert E et al (2011) The global
for the assessment of invasive species in large spread of Harmonia axyridis (Coleoptera: Coccinellidae):
countries distribution, dispersal and routes of invasion. Biocontrol
56:623–641
Cabrera AL (1971) Fitogeografı́a de la República Argentina.
Citizen science has been criticized because of lack of Bol Soc Argent Bot 14:1–42
accuracy of the data and the non-standardized sam- Camacho-Cervantes M, Ortega-Iturriaga A, del-Val E (2017)
pling effort (Dickinson et al. 2010). Nevertheless, this From effective biocontrol agent to successful invader: the
harlequin ladybird (Harmonia axyridis) as an example of
and other studies (e.g. Giovos et al. 2019; Grez et al. good ideas that could go wrong. PeerJ 5:e3296
2016; Hobson et al. 2017) demonstrate that it is a Chardon NI, Cornwell WK, Flint LE et al (2015) Topographic,
valuable tool for the assessment of invasive alien latitudinal and climatic distribution of Pinus coulteri:
species over large spatial areas. The accuracy of geographic range limits are not at the edge of the climate
envelope. Ecography 38:590–601
identification was high in our system (93% of the Dı́az S, Settele J, Brondı́zio E et al (2019) Summary for poli-
pictures sent by citizens were verified to be H. cymakers of the global assessment report on biodiversity
axyridis), but we are aware that our records might be and ecosystem services of the Intergovernmental Science-
biased to urban areas, and are not exhaustive. Never- Policy Platform on Biodiversity and Ecosystem Services.
https://www.ipbes.net/sites/default/files/downloads/spm_
theless, the records presented in this work allow us to unedited_advance_for_posting_htn.pdf
have a first approximation of the state of invasion by Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science
H. axyridis in Argentina, providing a baseline for as an ecological research tool: challenges and benefits.
future studies on its requirements and impacts, and call Annu Rev Ecol Evol Syst 41:149–172
Dickinson JL, Shirk J, Bonter D et al (2012) The current state of
for urgent national initiatives in the conservation of citizen science as a tool for ecological research and public
native ladybirds and other beneficial insects. engagement. Front Ecol Environ 10:291–297
Drury JP, Barnes M, Finneran AE et al (2019) Continent-scale
Acknowledgements We thank all citizens who contributed phenotype mapping using citizen scientists’ photographs.
data for this project. Jorge La Grotteria kindly provided records Ecography 42:1436–1445
from Ecoregistros. Damasia Lozada helped to edit the ms. VW Garcı́a MF, Becerra VC, Reising CE (1999) Harmonia axyridis
thanks PICT 2016-0157. HER was supported by the Natural Pallas (Coleoptera, Coccinelidae) Estudio biológico. Rev
Environment Research Council award number NE/R016429/1 Fac Cienc Agrar 31:85–91
123
Citizen science reveals the distribution of the invasive harlequin ladybird
Giovos I, Kleitou P, Poursanidis D et al (2019) Citizen-science Outhwaite CL, Powney GD, August TA et al (2019) Annual
for monitoring marine invasions and stimulating public estimates of occupancy for bryophytes, lichens and inver-
engagement: a case project from the eastern Mediter- tebrates in the UK, 1970–2015. Sci Data 6:1–12
ranean. Biol Invasions 21:3707–3721 Poutsma J, Loomans A, Aukema B et al (2007) Predicting the
Grez AA, Zaviezo T, Roy HE et al (2016) Rapid spread of potential geographical distribution of the harlequin lady-
Harmonia axyridis in Chile and its effects on local coc- bird, Harmonia axyridis, using the CLIMEX model. In:
cinellid biodiversity. Divers Distrib 22:982–994 Roy H, Wajnberg E (eds) From biological control to
Hiller T, Haelewaters D (2019) A case of silent invasion: Citizen invasion: the ladybird Harmonia axyridis as a model spe-
science confirms the presence of Harmonia axyridis cies. Springer, Berlin, pp 103–125
(Coleoptera, Coccinellidae) in Central America. PloS ONE Purse BV, Comont R, Butler A et al (2015) Landscape and
14:e0220082 climate determine patterns of spread for all colour morphs
Hobson EA, Smith-Vidaurre G, Salinas-Melgoza A (2017) of the alien ladybird Harmonia axyridis. J Biogeogr
History of nonnative monk parakeets in Mexico. PLoS 42:575–588
ONE 12:e0184771 R Core Team (2018) R: a language and environment for sta-
Hufbauer RA, Facon B, Ravigne V et al (2012) Anthropogeni- tistical computing. R Foundation for Statistical Comput-
cally induced adaptation to invade (AIAI): contemporary ing, Vienna. https://www.R-project.org/
adaptation to human-altered habitats within the native Roy H, Wajnberg E (2008) From biological control to invasion:
range can promote invasions. Evol Appl 5:89–101 the ladybird Harmonia axyridis as a model species. Bio-
Koch RL, Galvan TL (2008) Bad side of a good beetle: the North control 53:1–4
American experience with Harmonia axyridis. Biocontrol Roy HE, Brown PM, Adriaens T et al (2016) The harlequin
53:23–35 ladybird, Harmonia axyridis: global perspectives on inva-
Koch RL, Venette RC, Hutchison WD (2006) Invasions by sion history and ecology. Biol Invasions 18:997–1044
Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Saini ED (2004) Presencia de Harmonia axyridis (Pallas)
the western hemisphere: implications for South America. (Coleoptera: Coccinelidae) en la provincia de Buenos
Neotrop Entomol 35:421–434 Aires. Aspectos biológicos y morfológicos. Rev Investig
Majerus M, Strawson V, Roy H (2006) The potential impacts of Agropecu: RIA 33:151–160
the arrival of the harlequin ladybird, Harmonia axyridis Spear DM, Pauly GB, Kaiser K (2017) Citizen science as a tool
(Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol for augmenting museum collection data from urban areas.
Entomol 31:207–215 Front Ecol Evol 5:86
Montero G, Vignaroli L (2008) Un Coccinelı́do exótico (Har- Veran S, Piry S, Ternois V et al (2016) Modeling spatial
monia axyridis) invade los agroecosistema del sudeste de expansion of invasive alien species: relative contributions
Santa Fé. Rev Agromensajes 10:3–4 of environmental and anthropogenic factors to the
Olave A (2006) Estudios bioecológicos y de biodiversidad en spreading of the harlequin ladybird in France. Ecography
poblaciones de Quadraspidiotus perniciosus (Hemiptera: 39:665–675
Diaspididae) provenientes de montes frutales bajo sistemas
de producción orgánica y convencional. Niveles basales de
Publisher’s Note Springer Nature remains neutral with
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quén, p 162
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