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ORIGINAL ARTICLE
Insects as indicators of Key Biodiversity Areas
Dario Nania
1
| Maurizio Mei
1
| Michela Pacifici
1
| Carlo Rondinini
1
|
Alessio De Biase
1
| Denis Michez
2
| Pierfilippo Cerretti
1
1
Department of Biology and Biotechnology
“Charles Darwin”, Sapienza University of
Rome, Rome, Italy
2
Laboratory of Zoology, Research Institute for
Biosciences, University of Mons, Mons,
Belgium
Correspondence
Dario Nania, Department of Biology and
Biotechnology “Charles Darwin”, Sapienza
University of Rome, Viale dell’Università
32, 00185 Rome, Italy.
Email: dario.nania@uniroma1.it
Funding information
The European Union–NextGenerationEU,
Grant/Award Number: B83C22002950007;
The italian ministry of university and research,
Grant/Award Numbers: MUR PRIN2022, CUP,
B53D23011990006
Editor: Laurence Packer and
Associate Editor: Emily Heffernan
Abstract
1. Global change is affecting insect populations worldwide as species declines have
been reported from different areas of the planet.
2. Novel approaches such as the identification of Key Biodiversity Areas (KBAs) could
detect areas of high biodiversity value for insect populations. The KBA approach
relies on standardised criteria to identify important sites for biodiversity persis-
tence. The application of such criteria to large numbers of species would signifi-
cantly accelerate the KBA mapping process.
3. A systematic application of KBA criteria has not been tested on insects, and very lit-
tle is known about the efficiency and limits of such methodology.
4. We applied four KBA criteria in Italy to 28 species/subspecies of bumblebees and
identified potential KBAs for one species and three subspecies. Potential KBAs are
only partially nested within current Italian KBAs and the protected areas network.
When compared with potential KBAs of vertebrate species identified with the same
methodology, the degree of nesting is only 12%.
5. Our results provide evidence of a tendency of the KBA network to expand as more
species are assessed, raising questions about the ability of the criteria to detect
areas that truly are key for biodiversity and not just for specific taxa. We also high-
light issues regarding the use of KBA criteria on insects, such as data availability
and the use of subspecies. Further large-scale assessments of KBAs will reveal the
true potential of application of the KBA approach for insect conservation, and
whether it actually may slow down the loss of important units of their extraordinary
diversity.
KEYWORDS
bumblebees, Italy, KBA criteria, large-scale assessment
INTRODUCTION
Over recent years, an increasing number of studies reported evidence
of insect populations declining in different areas of the planet (Goul-
son, 2019; Homburg et al., 2019; Lewinsohn et al., 2022; Sánchez-
Bayo & Wyckhuys, 2019; Wagner et al., 2021). Although this negative
trend cannot be necessarily generalised as a global issue (Saunders
et al., 2020; Simmons et al., 2019), it is likely that the documented
cases reflect an alarming and widespread phenomenon with devastat-
ing consequences on Earth’s ecosystems. Large-scale assessments of
the global population status of insects can shed light on where and
which species are currently facing a decline, as well as the severity of
their extinction risk (Clausnitzer et al., 2009). However, despite their
extraordinary diversity and their key ecological roles, insects are rarely
Received: 9 July 2023 Accepted: 29 December 2023
DOI: 10.1111/icad.12712
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2024 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.
Insect Conserv Divers. 2024;1–10. wileyonlinelibrary.com/journal/icad 1
included in global assessments due to the poor knowledge of their dis-
tribution and the taxonomic/geographical biases of species records
(Rocha-Ortega et al., 2021).
Conservation assessments of invertebrate species usually focus
on the species level but are sometimes at higher taxonomic rank
(Heino & Soininen, 2007). Taxonomy is critical in biodiversity conser-
vation because international agreements, national environmental poli-
cies and conservation organisations rely on the assumption that
species are both fixed entities and identified correctly (Garnett &
Christidis, 2017; Thomson et al., 2018). However, insect systematics
still represents a major challenge for conservationists, as many insect
groups are poorly studied (Braby & Williams, 2016; Srivathsan
et al., 2023). In fact, only 8% of the globally described insect fauna has
been assessed under the criteria of the International Union for Nature
Conservation (IUCN, 2022). Further, it was shown that insects listed
in international conservation agreements such as the Bern Convention
and the Habitats Directive, are often better known, larger and wide-
spread (Leandro et al., 2017).
In a recent study, Chowdhury et al. (2023) estimated that a large
percentage of insect species are likely inadequately represented
within global protected areas. Furthermore, protected areas design
and management rarely focus on insects. In the present context of
wildlife decline, the use of rapid and automatized methods to identify
potentially relevant areas for conservation can accelerate the inclusion
of many species, which are normally left out of processes such as the
identification of Key Biodiversity Areas (KBAs) (Nania et al., 2023).
Such methods could also be combined with other automatized
approaches. For instance, species identification from large samples of
malaise traps (Wührl et al., 2022), can provide an additional layer
of information on the distribution of insect taxa and consequently
leading to more effective conservation planning. The KBA approach
aims at identifying sites that, if protected, can preserve the biodiver-
sity hosted within them. KBAs are identified through the application
of standard criteria (IUCN, 2016). Currently, with regard to identified
KBAs worldwide, only 6% of KBA trigger species are invertebrates,
for which KBAs are identified only under criteria A1, B1 and B2
(https://www.keybiodiversityareas.org/kba-data). A detailed descrip-
tion of these criteria is provided below. This evidence reveals an
important gap of knowledge on the distribution of insect KBAs. KBA
assessments for insect species are key to fill this gap.
This study is the first attempt to systematically apply KBA criteria
to multiple insect species over a defined geographic region. We
applied selected KBA criteria (A1, B1, B2 and B3, detailed in the
Materials and Methods section) to 28 European bumblebees (genus
Bombus Latreille, Hymenoptera: Apidae) following the methodology
presented in Nania et al. (2023). Although KBA criteria are supposed
to be applied at least to the species rank if genetic data are unavail-
able, we also selected subspecies with high geographic isolation and
distinct morphological features (Biella et al., 2017; Cappellari
et al., 2018; Dellicour et al., 2012; Intoppa et al., 2009; Martinet
et al., 2018; Rasmont et al., 2021), which represent putative separate
evolving biological units of conservation interest. We assessed the
presence of potential KBAs in Italy based on estimates of the global
population size of each taxon inferred through the use of area of habi-
tat (AOH) maps. We provided high-resolution AOH maps for all
28 species/subspecies analysed. Additionally, we estimated the per-
centage of identified potential KBAs that are already found in pro-
tected land within the administrative boundaries of Italy. Finally, we
address issues in the application of KBA criteria to insect taxa and
suggest possible improvements of the global KBA standards to enable
them to account for the complex biology and data availability of such
organisms.
MATERIALS AND METHODS
Distribution maps
We retrieved occurrence points for 28 Bombus species/subspecies
(Table 1) from the Atlas of European bees (Rasmont et al., 2015). The
species are endemic/subendemic of the European continent and their
global distribution can be estimated using data from Rasmont et al.
(2015), this information is crucial for the construction of AOH maps
and for KBA assessments (IUCN, 2016). We did not filter occurrence
points based on the date of record. Although including very old
records may not represent the current distribution of the species in
the most accurate way, proving the extinction of a species in a locality
is not easy. The fact that a species is not recorded in recent years
may depend on a lack of sampling as well as on other biological fac-
tors. As the methodology applied in this study represents the first
step of the KBA identification process (IUCN, 2016), a more conser-
vative approach is preferable. The second step, the KBA delineation
process, will define the distribution of true KBAs. The atlas provides
species distribution data in the form of centroids, but the original
occurrence points are available upon request to the authors. Most
records hold georeferenced coordinate data, although for 50% of spe-
cies the occurrence data of specific geographic areas (e.g., data from
Scandinavia and Britain) is only available in the form of centroid of a
grid. Grid size varies but the maximum grid size is 50 50 km. For
this reason, it would have been meaningless to derive a distribution
range following the mapping standard procedure provided by the
IUCN Red List guidelines (IUCN Standards and Petitions Commit-
tee, 2022). In order to derive a distribution range for each species
from its occurrence points, we used the freely accessible map
‘Admin-1 State and provinces’of the Natural Earth database
(nauralearthdata.com). The map contains data on internal first-order
administrative boundaries worldwide, with a resolution of 1:10 m. In
order to draw the boundaries of each species’geographical distribu-
tion, we performed an intersection between the species occurrence
points and the administrative boundaries map. We then retained only
the regions of the map intersected by the species occurrence points
(Figure 1). As for some species, the accuracy of data in certain areas
of their distribution is 2500 km
2
(50 50 km), and we also retained
administrative areas that were surrounded by areas touching occur-
rences and were ≤2500 km
2
, in order to avoid biases in our estimated
species distributions.
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The range maps derived from the intersection of species occur-
rence points and the administrative map here are considered an inter-
mediate step to produce the AOH maps. The produced range maps
can include areas where the species is not found. This is due to the
fact that even if a single species record falls within a large administra-
tive region, the whole region is retained as part of the range of the
species. However, when species’habitat requirements are applied to
map the available habitat within the range, these areas are signifi-
cantly reduced. For instance, the subspecies Bombus alpinus helleri
only occurs within a specific elevation range on the Alpine arch. The
occurrence points of this species crossed the lower region of Bayern,
which extends far north from the Alps, thus the whole region was
included in the range of the species. However, when the habitat of
the species was mapped according to its environmental requirements,
including its elevation range, the excess area was lost completely. A
scheme illustrating this process is available in Appendix S1.
Area of habitat maps
Following the procedure adopted by Nania et al. (2022), we increased
the information accuracy on the global distribution of the species by
producing high-resolution AOH maps for all 28 species/subspecies.
AOH maps show the habitat available to a species within its distribu-
tion range; they can be produced by combining the distribution range
with a land cover map and altitude data (Rondinini et al., 2011). In
order to generate the AOH maps, we linked the species to their habi-
tat using the CGLS-LC100 Copernicus Land Cover map categories as
habitat surrogates. The CGLS-LC100 map was produced by the EU
Earth observation program and can be accessed through the dedi-
cated portal (Buchhorn et al., 2019; Buchhorn et al., 2020). Informa-
tion about habitat preference and altitude limits of the species were
retrieved from unpublished records from the Zoological Museum of
the University of Rome, identified using Bumblekeys (Cappellari
TABLE 1 A list of the species and subspecies included in this study.
Species IUCN status Model performance Triggered KBA criteria
Bombus alpinus helleri Dalla Torre 1882 VU Positive
Bombus argillaceus (Scopoli, 1763) LC Positive
Bombus barbutellus (Kirby, 1802) LC Positive
Bombus bohemicus Seidl, 1838 DD Positive
Bombus brodmannicus delmasi (Tkalcu˚, 1973) EN A1
Bombus campestris (Panzer, 1801) LC Positive
Bombus cryptarum (Fabricius, 1775) LC Positive
Bombus flavidus Eversmann, 1852 LC Positive
Bombus gerstaeckeri Morawitz, 1882 VU Positive
Bombus inexspectatus (Tkalcu, 1963) EN Positive
Bombus konradini Reinig, 1965 EN Positive A1, B1
Bombus lapidarius (Linnaeus, 1758) LC Positive
Bombus lucorum aritzoensis Krüger, 1951 DD Negative B1
Bombus mendax Gerstaecker 1869 LC Positive
Bombus mesomelas Gerstaecker, 1869 LC Positive
Bombus monticola alpestris Vogt, 1909 DD Positive
Bombus monticola mathildis Martinet, Cornalba &
Rasmont 2016
DD B1
Bombus mucidus Gerstaecker, 1869 NT Positive
Bombus norvegicus Sparre Schneider, 1918 LC Negative
Bombus pratorum (Linnaeus, 1761) LC Positive
Bombus pyrenaeus Pérez, 1880 LC Positive
Bombus quadricolor (Lepeletier, 1832) LC Positive
Bombus ruderatus (Fabricius, 1775) LC Positive
Bombus rupestris (Fabricius, 1793) LC Positive
Bombus subterraneus (Linnaeus 1758) LC Positive
Bombus sylvestris (Lepeletier, 1832) LC Positive
Bombus vestalis (Geoffroi in Fourcroy, 1785) LC Positive
Bombus wurflenii Radoszkowski, 1860 LC Positive
Note: Species concepts refer to Rasmont et al. (2021). The IUCN Red List status is provided, as well as the outcome of the model performance evaluation
and the KBA criteria, which were triggered by the species.
INSECT Key Biodiversity Areas 3
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et al., 2018), as well as from a monograph on the biology of the spe-
cies (Rasmont et al., 2021). We selected 15 land-cover categories that
are present on the land surface of Italy and compiled species-habitat
association by linking the land cover categories to the habitat require-
ments of the species. Thus, only land-cover categories representing
habitat for the species were used to build the AOH maps. Each cate-
gory received a score of either 1 (if it represents habitat for the spe-
cies) or 0 (if it does not represent habitat for the species). Altitudinal
limits were established for each species, giving a minimum and maxi-
mum elevation at which the species can be found in the study area. A
table showing which land cover categories were linked to the species
habitat is available in Appendix S1. A base map containing both land
cover and altitude information was built following the same procedure
as Nania et al. (2023) (Figure 1). A detailed description of how the
base map was produced is given in Appendix S1. The base map has a
resolution of approximately 100 m at the equator, altitude data are
derived from the Shuttle Radar Topography Mission (USGS EROS
Archive, 2019). Finally, we reclassified the base map according to the
species’habitat requirements within their distribution range. To do
this, we masked the base map with the range map of each species,
keeping only land cover categories with an assigned score of 1 within
the elevation limits where the species occurs. Thus, all land cover cat-
egories occurring within the distribution range but not representing
habitat for the species were discarded. In order to validate our AOH
maps before applying the KBA criteria, we implemented a hypergeo-
metric distribution approach (Dahal et al., 2022), which has already
been used to validate AOH maps (Nania et al., 2023). This presence-
only based method describes the probability of a species’occurrence
point to fall within the AOH of a species, and thus validating the map.
To account for potential errors in our occurrence record dataset in
the georeferencing process, as well as other imperfections of our data
such as resolution limits of the AOH maps, we applied a buffer of
150 m to the occurrence points before the hypergeometric distribu-
tion test. We performed the test on the AOH maps only within the
national boundaries of Italy, as species-habitat requirements were
compiled according to the current knowledge on the biology of the
species in Italy. Moreover, we only tested AOH maps of species for
which we could retrieve at least five occurrence points in different
FIGURE 1 Explanatory scheme of the methodology. (a) Species occurrence points are used to delineate the range of the species. (b) The Area
of Habitat map is produced by mapping the species’habitat within its distribution range. (c) A grid is positioned on the AOH map to detect
potential KBAs and moved to three additional positions. The non-stationary position of the grid lowers the risk of omitting potential KBAs. (d) A
representation of the cell movement in the potential KBA identification process.
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localities within the species’distribution range. A detailed description
of how the habitat maps were generated and validated is available in
Appendix S1.
Potential KBA identification
We selected four KBA criteria that could be tested using AOH maps
as an estimate of the proportion of the species’global population size,
according to the global standards (IUCN, 2016). Furthermore, the four
criteria were previously tested on Italian reptiles and amphibians with
the same methodology (Nania et al., 2023), allowing a meaningful
comparison between our results and the potential KBAs for the Italian
herpetofauna. The selected criteria are the following: A1 (threatened
species), B1 (individual geographically restricted species), B2 (co-
occurring geographically restricted species) and B3 (geographically
restricted assemblages) (IUCN, 2016; KBA Standards and Appeals
Committee of IUCN SSC/WCPA, 2022). Criterion A1 refers to species
that have been assessed as threatened in the IUCN Red List of
Threatened Species. A site can activate A1 if it holds a significant pro-
portion of the global population size of a threatened species. The sig-
nificant proportion threshold to trigger A1 is described in the KBA
standards, and it depends on the level of threat that the species is
globally facing. Criterion B1 refers to species for which a significant
proportion of the global population is restricted to a particular site. B1
can be activated for sites that host ≥10% of the global population of a
species. Criterion B2 also refers to geographically restricted species;
a site can activate B2 if it hosts ≥1% of the global population of at
least two geographically restricted species. Criterion B3 can be acti-
vated if a site hosts ≥5 species that are restricted to a particular ecor-
egion or 10% of the species restricted to the ecoregion (IUCN, 2016;
KBA Standards and Appeals Committee of IUCN SSC/WCPA, 2022).
To identify potential KBAs under the selected criteria in Italy, we
produced a 10 10 km cell sized grid that entirely covered its admin-
istrative boundaries. This cell size was previously used to detect
potential KBAs for reptiles and amphibians in Italy and was suggested
to be more efficient than larger cells for this purpose (Nania
et al., 2023). We then followed the procedure adopted in Nania et al.
(2023) to scan the geographic surface and identify potential KBAs.
Land surface scanning was performed once for each species habitat
map. The grid captured the extent of species’AOH that was present
within each cell. In addition to its initial position, the grid was moved
by 5 km (half the size of a grid cell) along three axes: north, east and
north-east. This was done in order to prevent the grid from missing
potential KBAs due to its fixed position (Figure 1). The choice of how
to move the grid on the map is arbitrary. This approach allows us to
generate four different scans per species map, ensuring a reliable cov-
erage of potential KBAs on the map while keeping the computational
costs low. Subsequently, all cells holding a sufficient portion of the
habitat global extent and, thus, able to meet the threshold of at least
one of the selected KBA criteria were retained. Finally, for the species
that did trigger the KBA criteria, we extracted the portion of their
AOH map enclosed within the cells that met the KBA criteria thresh-
old, regardless of the position of the grid. This last step allowed us to
produce high-resolution potential KBA maps for each one of the
tested criteria.
Species/subspecies for which an official IUCN Red List global or
European assessment is lacking cannot be considered for the applica-
tion of A1 (threatened species), as stated in the global standards
(IUCN, 2016). In our case, A1 could potentially be triggered by three
species, as they are currently assessed as threatened in the IUCN Red
List (Table 1). However, we also included two subspecies while testing
for A1: B. alpinus helleni and B. brodmannicus delmasi.
While the three species were assessed as being threatened to
some degree by the IUCN Red List of Threatened Species
(IUCN, 2022; Quaranta et al., 2018), the two subspecies have not
been assessed. However, B. alpinus and B. brodmannicus are both
listed as threatened species at either global or European level (Table 1).
Thus, we assigned the same status to the subspecies as well, as the
level of threat must necessarily be the same at the very least. The
application of criterion B3 requires a measurement of the percentage
of global population confined to single ecoregions to define assem-
blages (IUCN, 2016). For this purpose, we used the WWF Palaearctic
Terrestrial Ecoregion map, which is freely available at the WWF portal
(https://www.worldwildlife.org/publications/terrestrial-ecoregions-of-
the-world, accessed on 4th June 2021).
Potential KBAs and other important sites for
biodiversity
A measure of nesting was performed between the potential KBA map
produced in this study using the selected criteria, and the follow-
ing maps:
•National protected areas of Italy
•Natura 2000 network in Italy
•Current KBA network in Italy
•The new potential KBA for Reptiles and Amphibians in Italy (Nania
et al., 2023)
The map of national protected areas was obtained from Feder-
parchi (Italian federation for natural parks and reserves) and is avail-
able upon request, while the Natura 2000 map was retrieved from the
European Environment Agency (EEA, 2021). Maps of the current
KBA network within the boundaries of Italy are available from the
Global Key Biodiversity Areas database upon request (https://www.
keybiodiversityareas.org/kba-data/request). Currently, 99.1% of
accepted KBAs in Italy are identified for avian species, no KBA was
identified for insects (https://www.keybiodiversityareas.org/kba-
data). The potential KBA map for Italian reptiles and amphibians was
taken from Nania et al. (2023). To test the percentage of nesting
between potential KBAs for different taxa, we only considered poten-
tial KBAs that were identified using cells of the same size as was
adopted in this study (10 10 km).
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RESULTS
Italian bumblebees AOH maps
We produced 28 high-resolution global AOH maps for 23 species and
5 subspecies of bumblebees occurring in Italy (Table 1). The mean
extent of habitat cover within the species ranges among the validated
maps is 16.4%. Maximum percentage of coverage is reached by
B. ruderatus with available habitat covering 62.3% of its range. The
lowest percentage is reached by the parasitic B. quadricolor, for which
habitat availability corresponds to 0.09% of its range. The hypergeo-
metric test revealed that 24 of 26 tested maps (92.3%) had a positive
performance and were evaluated as being significantly better than
expected from a random distribution model. Two maps were not bet-
ter than expected under randomness (B. norvegicus and B. lucorum arit-
zoensis); however, for these two species, we had the lowest number
of occurrence points, respectively, five and nine. For the rest of the
tested species, the available number of occurrence points was sub-
stantially higher (Appendix S1). A detailed description of the hyper-
geometric distribution test is available in Appendix S1. All maps are
available on the DRYAD repository: https://doi.org/10.5061/dryad.
stqjq2c82.
Potential KBAs for Italian bumblebees
Of the four selected criteria, only two were triggered by at least one
species (A1 and B1).
We identified potential KBAs for B. konradini and B. brodmannicus
delmasi under criterion A1. One species and two subspecies were able
to trigger potential KBAs under criterion B1: B. konradini, B. monticola
mathildis and B. lucorum aritzoensis. All three of them are endemic to
Italy. The total area covered by the detected potential KBAs is
1845 km
2
, corresponding to 0.6% of the total surface of Italy. The
majority of the new potential KBAs were identified in central Apen-
nines and western Alps, whereas small patches were found in the
island of Sardinia and northern Apennines (Figure 2).
The comparison with Italian protected areas revealed that 34.2%
of the potential KBAs found in this study are nested within national
protected areas, while 53.6% is included in the Natura 2000 network.
With regard to the currently accepted KBAs in Italy, 47.4% of our
potential KBAs for Bombus species are already included within these
sites. Maps showing the distribution of potential KBAs compared with
current KBAs, national protected areas and Natura 2000 sites are
available in Appendix S1. Finally, only 12.1% of them are nested
within areas that were identified as potential KBAs for reptiles and
FIGURE 2 Potential KBAs for Italian bumblebees. The map shows the distribution of the potential KBAs, as well as the activated criteria and
the species/subspecies that activated the KBAs.
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amphibians, following the same methodology (Nania et al., 2023).
Potential KBAs of both bumblebees and herpetofauna overlap mostly
in the Western Alps, while small areas of overlap are also found in
Sardinia.
DISCUSSION
Distribution data
The dataset of occurrence points used in this study was retrieved
from what likely is one of the most complete databases revealing the
global distribution of an insect group in Europe (Rasmont et al., 2015).
However, part of the occurrence extent of the species was deter-
mined by centroids of a grid, sometimes as large as 50 50 km. This
lack of accuracy can result in issues of reliability in the process of
determining the true range of a species, especially when the objective
is to meticulously map the availability of its habitat. Using coarse reso-
lution range maps could lead to commission errors, taking into consid-
eration areas where the species is thought to be present but is in fact
absent (Rondinini et al., 2006; Walter et al., 2008). Thus, like the inclu-
sion of historical records, this may lead to an overestimation of the
actual range of the species and consequently its habitat availability.
Despite the fact that the use of insect occurrence data has increased
over the years and large datasets are becoming available (Diniz-Filho
et al., 2010), for most insect species, information of occurrence is
scarce and lacking accuracy (Rocha-Ortega et al., 2021). Identifying
KBAs requires complete and reliable occurrence data (IUCN, 2016), as
well as any macroecological analysis with conservation purpose. This
evidence highlights the urgency of assembling and sharing accessible
databases on the distribution of insects, as this will facilitate their
inclusion in large scale conservation assessments such as the one pre-
sented in this study. Nevertheless, producing high-resolution AOH
maps instead of using the whole species range proves to be efficient
in reducing the total area under examination, as on average the per-
centage of the entire range covered by habitat was found to
be 15.5%.
AOH maps are based on land cover and altitudinal limits (Brooks
et al., 2019), but do not take into account the latitudinal gradient.
This aspect also might influence the reliability of our maps, as altitudi-
nal limits of the species can vary substantially along the latitude gra-
dient. Here, we aimed at identifying potential KBAs for the species
within the geographical boundaries of Italy, and thus, the altitudinal
limits were set according to knowledge of the species in Italy. How-
ever, the application of KBA criteria requires an estimate of the global
population size inferred through the AOH map. For this reason, the
AOH maps were built across the global range of the species.
Although AOH maps are built through the application of the same
species’habitat requirements throughout their range, taking into con-
sideration the variation of altitudinal range across the latitudinal gra-
dient would allow a more reliable assessment of the species’global
population.
Potential KBAs
Although we tested four different KBA criteria on our data, we found
potential KBAs triggered by only two of them, A1 and B1 (Table 1).
These two criteria can only be triggered by a single species, while the
remaining two tested criteria (B2 and B3) need to be triggered by a
higher number of species (IUCN, 2016). This evidence suggests that
criteria based on single species assessments are more likely to be trig-
gered in a multi-criteria analysis such as the one presented in this
study. The same trend was observed in a previous study that system-
atically applied the four criteria to reptiles and amphibians in Italy
(Nania et al., 2023).
As shown in our results, potential KBAs were detected for one
species and four subspecies (Table 1), all of them endemic to Italy.
The subject of whether or not subspecies should be considered valu-
able biological units in conservation biology, and how, has been dis-
cussed extensively over the years (Braby et al., 2012; Haig
et al., 2006; Patten, 2015; Phillimore & Owens, 2006). For inverte-
brates in particular, it has been suggested how subspecies repre-
sented by isolated allopatric populations, with a distinct phenotype
which is correlated with an evolutionary independence should be
evaluated as significant biodiversity units for conservation (Braby
et al., 2012; Ghisbain et al., 2021). The global standards for the identi-
fication of KBAs allow the detection of KBAs for subspecies solely
through an assessment of their distinct genetic diversity (IUCN, 2016;
KBA Standards and Appeals Committee of IUCN SSC/WCPA, 2022).
Our suggestion in this regard is to allow other aspects that character-
ise subspecies to play a role in the identification of KBAs, such as geo-
graphical isolation, which can promote reproductive isolation and
evolutionary divergence (Worsham et al., 2017). This would allow
rapid assessments for many subspecies for which genetic data are still
missing or not easily accessible, avoiding the loss of important biodi-
versity units through timely conservation actions. For instance,
B. monticola mathildis was able to trigger potential KBAs under crite-
rion B1 (individual geographically restricted species) in the northern
Apennines (Figure 2). Previous genetic analysis using mitochondrial
cytochrome oxidase subunit 1 (COI) suggested that B. monticola
mathildis is closer to B. konradini than to the populations of
B. monticola in the Alps (Martinet et al., 2018), providing evidence
of some degree of isolation and divergence of this population. Includ-
ing such subspecies in KBA assessments can highlight the fragility of
their global population as determined by habitat availability, distinct
morphological characters, and isolated and restricted distribution. Ulti-
mately leading to rapid conservation actions if needed.
The only species that triggered both A1 and B1 is B. konradini
(Figure 2). This species is known to be rare and of particular concern,
as it is endemic to a restricted region in the central Apennines and is
found almost only above 1800 m of elevation (Rasmont et al., 2021).
All of the B. konradini habitat mapped in this study was included in
potential KBAs in the central Apennines, and it represents the only
potential KBAs detected in central Italy for the species tested in this
study (Figure 2). This result suggests it is likely that at least part of the
INSECT Key Biodiversity Areas 7
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potential KBAs identified for this species could reflect actual KBAs
through the proposal process (KBA Standards and Appeals Committee
of IUCN SSC/WCPA, 2022). However, we stress that the areas identi-
fied through our systematic approach must necessarily be considered
as potential KBAs and that the actual KBA area can be smaller and dif-
ferently shaped.
The nesting analysis revealed that a large portion (65.8%) of the
total area found in this study is not included in national protected
areas, and almost half of the area (46.4%) is left out of Natura 2000
sites. In this regard, our potential KBAs map highlights areas that are
potentially important for the preservation of the species hosted by
them, and for which some degree of protection may be needed. The
comparison with the current KBA network in Italy suggests that, if
the potential KBAs found in this study were to be confirmed, more
than 30% of their total extent should be integrated as an addition to
Italian KBAs. A similar trend was observed for reptiles and amphibians,
for which only 18% of the potential KBAs were already included in
the current KBA network (Nania et al., 2023). Moreover, only 12.1%
of the potential KBAs for bumblebees were found to be nested within
those for reptiles and amphibians using the same methodology. Con-
sidering the very limited number of species tested in both studies,
respectively, 28 bumblebees and 59 species of reptiles and amphib-
ians (Nania et al., 2023), if the potential new KBAs were found to
be actually present, the Italian KBA network would expand signifi-
cantly across the country’s geographic surface. Currently, 99.1% of
Italian KBAs are triggered by bird species (https://www.
keybiodiversityareas.org/kba-data). It appears that, as more taxa are
tested the total KBA area tends to increase. Consequently, if large
numbers of both animal and plant species were tested, this phenome-
non could lead to geographical over-expansion of the KBA network
and a loss of relevance of these areas, as their use to inform conserva-
tion and land use planning would become more complicated.
Overall, several issues emerged regarding the implementation of
insect taxa for the identification of KBAs through a systematic
approach. First, the lack of accuracy of insect georeferenced data and
imprecision in delineating a geographic range for the species implies
assumptions that can lead to an overestimation (or underestimation)
of the actual global population size of a species. We highlight the
importance and necessity of assembling large-scale dataset for insect
taxa avoiding approximations using low-resolution grids. These data-
set should be available upon request for research purposes without
loss of the original occurrence data resolution. This would lead to a
progressive inclusion of insect taxa in large-scale assessments for con-
servation purposes as well as to an increase of consideration of such
taxa when developing methodologies that serve the purpose of biodi-
versity conservation. We also discussed the issue of subspecies inclu-
sion in KBA assessments. Running appropriate population genetics
analysis to test for distinct genetic diversity as the only way to acti-
vate KBAs for subspecies is not a realistic approach. For most taxa,
such data are not available or not easily accessible. Insect taxonomy is
complex, thus the level of uncertainty of whether or not a subspecies
represents an evolutionary independent unit worth of being consid-
ered for KBA assessments is high. However, insect populations are
declining at a worrying rate (Goulson, 2019; Homburg et al., 2019;
Lewinsohn et al., 2022; Wagner et al., 2021), and many relevant sub-
species may be lost long before genetic data are finally available.
Other factors such as geographic isolation can be used to include
insect subspecies in KBA assessments. Finally, the observed tendency
of expansion of the KBA network as more species are tested raises
questions about the efficiency of the KBA approach in identifying
areas that truly are key for biodiversity and not only for a limited sub-
set of it.
AUTHOR CONTRIBUTIONS
Dario Nania: Software; conceptualization; investigation; writing –orig-
inal draft; validation; methodology; data curation; formal analysis.
Maurizio Mei: Conceptualization; data curation; investigation.
Michela Pacifici: Writing –review and editing; methodology; visuali-
zation. Carlo Rondinini: Methodology; conceptualization. Alessio De
Biase: Writing –review and editing. Denis Michez: Data curation.
Pierfilippo Cerretti: Supervision; conceptualization; data curation;
writing –review and editing; investigation.
ACKNOWLEDGEMENTS
This work received support from The European Union–NextGenera-
tionEU as part of the National Biodiversity Future Center, Italian
National Recovery and Resilience Plan (NRRP) Mission 4 Component
2 Investment 1.4 (CUP: B83C22002950007).
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are openly available in
DRYAD at https://doi.org/10.5061/dryad.stqjq2c82.
ORCID
Dario Nania https://orcid.org/0000-0002-2144-9101
Denis Michez https://orcid.org/0000-0001-8880-1838
REFERENCES
Biella, P., Bogliani, G., Cornalba, M., Manino, A., Neumayer, J.,
Porporato, M. et al. (2017) Distribution patterns of the cold adapted
bumblebee Bombus alpinus in the Alps and Hints of an Uphill Shift
(Insecta: Hymenoptera: Apidae). Journal of Insect Conservation, 21(2),
357–366. Available from: https://doi.org/10.1007/s10841-017-
9983-1
Braby, M.F., Eastwood, R. & Murray, N. (2012) The subspecies concept in
butterflies: has its application in taxonomy and conservation biology
outlived its usefulness? Biological Journal of the Linnean Society, 106
(4), 699–716. Available from: https://doi.org/10.1111/j.1095-8312.
2012.01909.x
Braby, M.F. & Williams, M.R. (2016) Biosystematics and conservation biol-
ogy: critical scientific disciplines for the management of insect bio-
logical diversity. Austral Entomology, 55(1), 1–17. Available from:
https://doi.org/10.1111/aen.12158
Brooks, T.M., Pimm, S.L., Akçakaya, H.R., Buchanan, G.M., Butchart, S.H.
M., Foden, W. et al. (2019) Measuring terrestrial area of habitat
(AOH) and its utility for the IUCN Red List. Trends in Ecology and
8NANIA ET AL.
17524598, 0, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/icad.12712 by Dario Nania - University Di Roma La Sapienza , Wiley Online Library on [17/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Evolution, 34(11), 977–986. Available from: https://doi.org/10.1016/
j.tree.2019.06.009
Buchhorn, M., Smets, B., Bertels, L., de Roo, B., Lesiv, M., Tsendbazar, N.E.
et al. (2020) Copernicus Global Land Service: Land Cover 100m: Version
3 Globe 2015–2019: Product User Manual. Geneve: Zenodo. https://
doi.org/10.5281/zenodo.3938963
Cappellari, A., Mei, M., Lopresti, M. & Cerretti, P. (2018) BumbleKey: an
interactive key for the identification of bumblebees (Hymenoptera,
Apidae) of Italy and Corsica. ZooKeys, 784, 127–138. Available from:
https://doi.org/10.3897/zookeys.784.25765
Chowdhury, S., Zalucki, M.P., Hanson, J.O., Tiatragul, S., Green, D.,
Watson, J.E. et al. (2023) Three-quarters of insect species are insuffi-
ciently represented by protected areas. One Earth, 6(2), 139–146.
Clausnitzer, V., Kalkman, V.J., Ram, M., Collen, B., Baillie, J.E., Bedjaniˇ
c, M.
et al. (2009) Odonata enter the biodiversity crisis debate: the first
global assessment of an insect group. Biological Conservation, 142(8),
1864–1869. Available from: https://doi.org/10.1016/j.biocon.2009.
03.028
Dahal, P.R., Lumbierres, M., Butchart, S.H.M., Donald, P.F. & Rondinini, C.
(2022) A validation standard for area of habitat maps for terrestrial
birds and mammals. Geoscientific Model Development, 15, 5093–
5105. Available from: https://doi.org/10.5194/gmd-15-5093-2022
Dellicour, S., de Jonghe, R., Roelants, D. & Michez, D. (2012) Oligolectisme
de Bombus brodmannicus delmasi Tkalcu˚, 1973 (Hymenoptera, Api-
dae): observations et analyses. Osmia,5,8–11. Available from:
https://doi.org/10.47446/OSMIA5.4
Diniz-Filho, J.A.F., de Marco, P. & Hawkins, B.A. (2010) Defying the curse
of ignorance: perspectives in insect macroecology and conservation
biogeography. Insect Conservation and Diversity, 3(3), 172–179. Avail-
able from: https://doi.org/10.1111/j.1752-4598.2010.00091.x
EEA. (2021) European environmental agency. Natura 2000 End 2021.
Available from: https://www.eea.europa.eu/data-and-maps/data/
natura-14/natura-2000-spatial-data [Accessed 8th February 2022].
Garnett, S.T. & Christidis, L. (2017) Taxonomy anarchy hampers conserva-
tion. Nature, 546(7656), 25–27. Available from: https://doi.org/10.
1038/546025a
Ghisbain, G., Martinet, B., Wood, T.J., Przybyla, K., Cejas, D., Gérard, M.
et al. (2021) A worthy conservation target? Revising the status of the
rarest bumblebee of Europe. Insect Conservation and Diversity, 14(5),
661–674.
Goulson, D. (2019) The insect apocalypse, and why it matters. Current Biol-
ogy, 29(19), R967–R971. Available from: https://doi.org/10.1016/j.
cub.2019.06.069
Haig, S.M., Beever, E.A., Chambers, S.M., Draheim, H.M., Dugger, B.D.,
Dunham, S. et al. (2006) Taxonomic considerations in listing subspe-
cies under the U.S. Endangered Species Act. Conservation Biology,20
(6), 1584–1594. Available from: https://doi.org/10.1111/j.1523-
1739.2006.00530.x
Heino, J. & Soininen, J. (2007) Are higher taxa adequate surrogates for
species-level assemblage patterns and species richness in stream
organisms? Biological Conservation, 137(1), 78–89. Available from:
https://doi.org/10.1016/j.biocon.2007.01.017
Homburg, K., Drees, C., Boutaud, E., Nolte, D., Schuett, W., Zumstein, P.
et al. (2019) Where have all the beetles gone? Long-term study
reveals carabid species decline in a nature reserve in northern Ger-
many. Insect Conservation and Diversity, 12(4), 268–277. Available
from: https://doi.org/10.1111/icad.12348
Intoppa, F., Piazza, M.G., Bolchi Serini, G. & Cornalba, M. (2009) Bombi.
Guida al riconoscimento delle specie italiane. CRA—Unità di Ricerca
di Apicoltura e Bachicoltura Bologna.
IUCN. (2016) A global standard for the identification of key biodiversity areas,
1st edition. Gland, Switzerland: IUCN.
IUCN. (2022) IUCN Red List of threatened species. Available from:
https://www.iucnredlist.org/en [Accessed 12th October 2022]
IUCN Standards and Petitions Committee. (2022) Guidelines for using the
IUCN Red List categories and criteria. Version 15.1. Prepared by the
Standards and Petitions Committee. Available from: https://www.
iucnredlist.org/documents/RedListGuidelines.pdf
KBA Standards and Appeals Committee of IUCN SSC/WCPA. (2022)
Guidelines for using a global standard for the identification of Key
Biodiversity Areas. Version 1.2. Gland, Switzerland: IUCN.
Leandro, C., Jay-Robert, P. & Vergnes, A. (2017) Bias and perspectives in
insect conservation: a European scale analysis. Biological Conserva-
tion, 215, 213–224. Available from: https://doi.org/10.1016/j.
biocon.2017.07.033
Lewinsohn, T.M., Agostini, K., Lucci Freitas, A.V. & Melo, A.S. (2022) Insect
decline in Brazil: an appraisal of current evidence. Biology Letters,18
(8), 20220219. Available from: https://doi.org/10.1098/rsbl.2022.
0219
Martinet, B., Lecocq, T., Brasero, N., Biella, P., Urbanová, K., Valterová, I.
et al. (2018) Following the cold: geographical differentiation between
interglacial refugia and speciation in the arcto-alpine species com-
plex Bombus monticola (Hymenoptera: Apidae). Systematic Entomol-
ogy, 43(1), 200–217. Available from: https://doi.org/10.1111/syen.
12268
Nania, D., Ficetola, F., Falaschi, M., Pacifici, M., Lumbierres, M. &
Rondinini, C. (2023) An automated approach for systematic detec-
tion of key biodiversity areas. bioRxiv. Available from: https://doi.
org/10.1101/2023.06.30.547173
Nania, D., Lumbierres, M., Ficetola, G.F., Falaschi, M., Pacifici, M. &
Rondinini, C. (2022) Maps of area of habitat for Italian amphibians
and reptiles. Nature Conservation, 49, 117–129. Available from:
https://doi.org/10.3897/natureconservation.49.82931
Patten, M.A. (2015) Subspecies and the philosophy of science. The Auk,
132(2), 481–485. Available from: https://doi.org/10.1642/AUK-15-
1.1
Phillimore, A.B. & Owens, I.P.F. (2006) Are subspecies useful in evolution-
ary and conservation biology? Proceedings of the Royal Society B: Bio-
logical Sciences mitochondrial cytochrome oxidase subunit 1, 273
(1590), 1049–1053. Available from: https://doi.org/10.1098/rspb.
2005.3425
Quaranta, M., Cornalba, M., Biella, P., Comba, M., Battistoni, A.,
Rondinini, C., & Teofili, C. (2018). Red list IUCN of the Italian threat-
ened bees [Lista Rossa IUCN delle api italiane minacciate]”. Comitato
Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio
e del Mare, Roma.
Rasmont, P., Franzén, M., Lecocq, T., Harpke, A., Roberts, S., Biesmeijer, J.
C. et al. (2015) Climatic risk and distribution atlas of european bum-
blebees. BioRisk, 10, 1–236. Available from: https://doi.org/10.
3897/biorisk.10.4749
Rasmont, P., Ghisbain, G. & Terzo, M. (2021) Bumblebees of Europe and
neighbouring regions—Hymenoptera of Europe 3. NAP Editions, Ver-
rières-le-Buisson, France, 632 pp.
Rocha-Ortega, M., Rodriguez, P. & C
ordoba-Aguilar, A. (2021) Geographi-
cal, temporal and taxonomic biases in insect GBIF data on biodiver-
sity and extinction. Ecological Entomology, 46(4), 718–728. Available
from: https://doi.org/10.1111/een.13027
Rondinini, C., Di Marco, M., Chiozza, F., Santulli, G., Baisero, D.,
Visconti, P. et al. (2011) Global habitat suitability models of terrestrial
mammals. Philosophical Transactions of the Royal Society B: Biological
Sciences, 366(1578), 2633–2641. Available from: https://doi.org/10.
1098/rstb.2011.0113
Rondinini, C., Wilson, K.A., Boitani, L., Grantham, H. & Possingham, H.P.
(2006) Tradeoffs of different types of species occurrence data for
use in systematic conservation planning. Ecology Letters, 9(10),
1136–1145. Available from: https://doi.org/10.1111/j.1461-0248.
2006.00970.x
Sánchez-Bayo, F. & Wyckhuys, K.A.G. (2019) Worldwide decline of the
entomofauna: a review of its drivers. Biological Conservation, 232, 8–
27. Available from: https://doi.org/10.1016/j.biocon.2019.01.020
Saunders, M.E., Janes, J.K. & O’Hanlon, J.C. (2020) Moving on from the
insect apocalypse narrative: engaging with evidence-based insect
INSECT Key Biodiversity Areas 9
17524598, 0, Downloaded from https://resjournals.onlinelibrary.wiley.com/doi/10.1111/icad.12712 by Dario Nania - University Di Roma La Sapienza , Wiley Online Library on [17/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
conservation. BioScience, 70(1), 80–89. https://doi.org/10.1093/
biosci/biz143
Simmons, B.I., Balmford, A., Bladon, A.J., Christie, A.P., De Palma, A.,
Dicks, L.V. et al. (2019) Worldwide insect declines: an important
message, but interpret with caution. Ecology and Evolution, 9(7),
3678–3680. Available from: https://doi.org/10.1002/ece3.5153
Srivathsan, A., Ang, Y., Heraty, J.M., Hwang, W.S., Jusoh, W.F., Kutty, S.N.
et al. (2023) Covergence of dominance and neglect in flying insect
diversity. Nature Ecology & Evolution, 7, 1012–1021. Available from:
https://doi.org/10.1038/s41559-023-02066-0
Thomson, S.A., Pyle, R.L., Ahyong, S.T., Alonso-Zarazaga, M., Ammirati, J.,
Araya, J.F. et al. (2018) Taxonomy based on science is necessary for
global conservation. PLOS Biology, 16, e2005075. Available from:
https://doi.org/10.1371/journal.pbio.2005075
USGS EROS Archive. (2019) Digital elevation—shuttle radar topography
mission (SRTM) 1 Arc-Second Global.
author>Wagner, D.L., Grames, E.M., Forister, M.L., Berenbaum, M.R. &
Stopak, D. (2021) Insect decline in the anthropocene: death by a
thousand cuts. Proceedings of the National Academy of Sciences, 118
(2), e2023989118. Available from: https://doi.org/10.1073/pnas.
2023989118
Walter, J., Sekercioglu, C.H. & Watson, J.E.M. (2008) Ecological correlates
and conservation implications of overestimating species geographic
ranges. Conservation Biology, 22(1), 110–119. Available from: https://
doi.org/10.1111/j.1523-1739.2007.00847.x
Worsham, M.L.D., Julius, E.P., Nice, C.C., Diaz, P.H. & Huffman, D.G.
(2017) Geographic isolation facilitates the evolution of reproductive
isolation and morphological divergence. Ecology and Evolution, 7(23),
10278–10288. Available from: https://doi.org/10.1002/ece3.3474
Wührl, L., Pylatiuk, C., Giersch, M., Lapp, F., von Rintelen, T., Balke, M. et al.
(2022) DiversityScanner: robotic handling of small invertebrates with
machine learning methods. Molecular Ecology Resources, 22(4), 1626–
1638. Available from: https://doi.org/10.1111/1755-0998.13567
SUPPORTING INFORMATION
Additional supporting information can be found online in the Support-
ing Information section at the end of this article.
Appendix S1. Supporting Information.
How to cite this article: Nania, D., Mei, M., Pacifici, M.,
Rondinini, C., De Biase, A., Michez, D. et al. (2024) Insects as
indicators of Key Biodiversity Areas. Insect Conservation and
Diversity,1–10. Available from: https://doi.org/10.1111/icad.
12712
10 NANIA ET AL.
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