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Citizen Science Reveals The Distribution of The Invasive

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Biol Invasions

https://doi.org/10.1007/s10530-020-02312-7 (0123456789().,-volV)
( 01234567
89().,-volV)

INVASION NOTE

Citizen science reveals the distribution of the invasive


harlequin ladybird (Harmonia axyridis Pallas) in Argentina
Victoria Werenkraut . Florencia Baudino . Helen E. Roy

Received: 24 September 2019 / Accepted: 2 July 2020


Ó Springer Nature Switzerland AG 2020

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

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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)

Methods reinforced the survey creating a flyer with summary


information of the project which we disseminated on
To gather citizen science records we developed a Facebook, Instagram and Twitter, and we added two
website (https://sites.google.com/a/comahue-conicet. additional ways of reporting records: (4) a WhatsApp
gob.ar/vam) with information about the species and number; and (5) a Facebook page (https://www.
how to identify it, and we offered different ways for facebook.com/vaquita.asiaticamulticolor); also we
reporting data: (1) an iNaturalist project (https://www. circulated new e-mails to Institutions and scientists
inaturalist.org/projects/vaquita-asiatica-multicolor); targeting regions lacking records. In addition, we
(2) a Google form; and (3) an institutional email. In received records and specimens from colleagues and
early June 2018 we widely promoted our project by other acquaintances, which we classified as ‘‘Other
sending more than 100 emails with a brief description Methods’’.
and the link to the website to people from universities, We asked citizens to report the date and location of
scientific institutes, and scientific societies in Argen- the sighting (as accurately as possible) and to send a
tina, and we specifically asked them to widely dis- picture in any life stage (larva, pupa or adult). For
seminate the information to all their community records lacking geographic coordinates, we approxi-
members (not only within academia). We initially mated them by using Google Maps searching for the
encouraged the use of iNaturalist in order to have open address, city, or locality name. We used the pictures to
and georeferenced data. In December 2018 we verify the species identity. When it was not possible to

123
V. Werenkraut et al.

confirm the identification, we asked the citizens to


send a new picture, if possible. Only records with
verified pictures were included in our database. We
used QGIS 2.18 (Team, QGIS Development) and R
3.4.4 (R Core Team 2018) to analyse data.

Results and discussion

From June 2018 to July 2019 we received 370 records


from 275 citizens. We also included in our database 17
records from eight citizens uploaded to iNaturalist
previous to the promotion of our project, totalizing
387 records and 279 citizens. Pictures allowed us to
verify 93% of submitted records (N = 361) to be H.
axyridis. Seventy-eight per cent of these records
(N = 283) were geo-referenced by the citizens (59%)
or were sent with precise addresses (19%) allowing us Fig. 2 Number of records received (dark grey) and number of
citizens reporting records (light grey) by way of reporting. These
to add accurate geo-references. Geographical coordi- numbers were divided by the number of days each method was
nates of the remaining records were approximated active (N = 425 days for iNaturalist, Email, Google Form and
by B 10 km2 (11%), between 10 to 50 km2 (5.5%), Other methods, and N = 235 days for WhatsApp and Facebook)
and [ 50 km2 (5.5%) depending on the information
sent about the locality of the record. Additionally, one iNaturalist website, which came from eight users. By
citizen alerted us to the records of H. axyridis in the end of July 2019, the number of users was 93,
Ecoregistros (http://www.ecoregistros.org), an and * 70% of them created their profiles after the
Argentinean naturalists website, from which we got beginning of our project. It is reasonable to think that
182 additional records from 2007 to 2019, leading to a at least some of these citizens registered because of our
total of 543 records of the species in Argentina request and thus, our project might also be promoting
(Fig. 1b; Online Resource 2, Table 2b). the use of iNaturalist in Argentina.
Encouraging the use of iNaturalist and other citizen
Preferred ways of sending records science platforms is particularly relevant because it
provides valuable open data which can be easily used
Citizens sent records using all the proposed methods. by the scientific community worldwide beyond the
Most of the validated records came from iNaturalist objective of a particular project. Citizen science open
(N = 152) and WhatsApp (N = 86), followed by data platforms have shown to be a valuable source of
email (N = 45), and Facebook (N = 27), while Google records of many types of organisms for many fields of
Forms and Other Methods contributed less than 10% research. For instance, data available in these plat-
of the records (N = 16 and N = 18, respectively). forms have been used to generate models to under-
When we took into account the total number of days stand current and future distribution and status of
each method was available, the order of email and plants and animals (Chardon et al. 2015; Outhwaite
Facebook were slightly reverted. In addition, iNatu- et al. 2019), to analyse phenotypic variation of insect
ralist and WhatsApp showed a similar frequency of species (Drury et al. 2019), and to bolster museum
use (Fig. 2), indicating that both methods are good collections data of native and invasive reptiles and
candidates for future citizen science projects within amphibians particularly from urban and suburban
Argentina. The number of citizens was similar areas (Spear et al. 2017) among many other cases.
between iNaturalist (N = 89) and WhatsApp
(N = 84), but iNaturalist users tended to send more
than one record (Fig. 2). Before our project, there were
only 17 records of H. axyridis in Argentina in the

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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

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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:
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Publisher’s Note Springer Nature remains neutral with
algunos constituyentes del sistema antioxidante. Facultad
regard to jurisdictional claims in published maps and
de Ingenierı́a Universidad Nacional del Comahue, Neu-
institutional affiliations.
quén, p 162

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