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Distribution patterns of the cold adapted bumblebee Bombus alpinus in the Alps and hints of an uphill shift (Insecta: Hymenoptera: Apidae)

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Climate change is threatening species and habitats. Altitudinal shifts uphill and negative population trends are commonly observed in altitude-related taxa. The bumblebee Bombus alpinus (Linnaeus, 1758) has a disjoint distribution restricted to Fennoscandia and the Alps, and is considered threatened. We studied the ecology and distribution of B. alpinus in the Alps, where the endemic subspecies Bombus alpinus helleri Dalla Torre 1882 is found, as a case-model because of its rarity, habitat, and mutual dependence with the ecosystem for pollination and resources. We developed species distribution models including both climatic and habitat variables to obtain the surface suitable for this subspecies and quantified its protected portion. Our analyses indicate that this bumblebee is restricted to the upper altitudes and has a narrow niche mainly related to the presence of glaciers, the cool temperature, a low temperature variation, and a specific range of precipitation. A strong altitudinal shift is also taking place probably due to climate change. After years of no changes in altitudinal distribution, its lowest altitudinal limit has moved up 479 m since the year 1984, while its upper altitudinal limit has remained unchanged. Over half of the suitable area in the Alps is included within protected areas, but conservation has not been planned yet. However, rare species with narrow niche, such as B. alpinus, are highly threatened by climate change. Potential short-term mitigation actions are discussed, including exchange of males between locations and integral protection of prairies in the vicinity of glaciers.
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J Insect Conserv (2017) 21:357–366
DOI 10.1007/s10841-017-9983-1
ORIGINAL PAPER
Distribution patterns ofthecold adapted bumblebee Bombus
alpinus intheAlps andhints ofanuphill shift (Insecta:
Hymenoptera: Apidae)
PaoloBiella1,2 · GiuseppeBogliani3· MaurizioCornalba4· AuloManino5·
JohannNeumayer6· MarcoPorporato5· PierreRasmont7· PietroMilanesi3,8
Received: 23 August 2016 / Accepted: 25 April 2017 / Published online: 27 April 2017
© Springer International Publishing Switzerland 2017
and resources. We developed species distribution models
including both climatic and habitat variables to obtain the
surface suitable for this subspecies and quantified its pro-
tected portion. Our analyses indicate that this bumblebee
is restricted to the upper altitudes and has a narrow niche
mainly related to the presence of glaciers, the cool tempera-
ture, a low temperature variation, and a specific range of
precipitation. A strong altitudinal shift is also taking place
probably due to climate change. After years of no changes
in altitudinal distribution, its lowest altitudinal limit has
moved up 479m since the year 1984, while its upper altitu-
dinal limit has remained unchanged. Over half of the suit-
able area in the Alps is included within protected areas,
but conservation has not been planned yet. However, rare
species with narrow niche, such as B. alpinus, are highly
threatened by climate change. Potential short-term miti-
gation actions are discussed, including exchange of males
between locations and integral protection of prairies in the
vicinity of glaciers.
Keywords Climate change· Specialist· Rare species·
Species distribution modelling· Altitudinal shift·
Conservation
Introduction
Global change is currently threatening many species
(Thomas etal. 2004). Together with land use change (Mar-
tins et al. 2014; Jha 2015), agricultural practices (Oller-
ton etal. 2014; Rundlöf et al. 2015), and new pathogens
(Smith etal. 2006; Cameron et al. 2011), climate change
affects the survival of endangered species and could even
cause extinctions (e.g. Parmesan and Yohe 2003; Thomas
et al. 2004). As pointed out by the International Panel
Abstract Climate change is threatening species and
habitats. Altitudinal shifts uphill and negative population
trends are commonly observed in altitude-related taxa. The
bumblebee Bombus alpinus (Linnaeus, 1758) has a dis-
joint distribution restricted to Fennoscandia and the Alps,
and is considered threatened. We studied the ecology and
distribution of B. alpinus in the Alps, where the endemic
subspecies Bombus alpinus helleri Dalla Torre 1882 is
found, as a case-model because of its rarity, habitat, and
mutual dependence with the ecosystem for pollination
Electronic supplementary material The online version of this
article (doi:10.1007/s10841-017-9983-1) contains supplementary
material, which is available to authorized users.
* Paolo Biella
paolo.biella@entu.cas.cz
1 Department ofZoology, Faculty ofScience, University
ofSouth Bohemia, Branišovská 31, 37005ČeskéBudějovice,
CzechRepublic
2 Biology Centre oftheAcademy ofSciences oftheCzech
Republic, v.v.i., Institute ofEntomology, Branišovská 31,
37005ČeskéBudějovice, CzechRepublic
3 Department ofEarth andEnvironmental Sciences, University
ofPavia, via Adolfo Ferrata 9, 27100Pavia, Italy
4 Department ofMathematics, University ofPavia, via Ferrata
5, 27100Pavia, Italy
5 Department ofAgricultural, Forest andFood Sciences
(DISAFA), University ofTorino, Largo Paolo Braccini 2,
10095Grugliasco, TO, Italy
6 Obergrubstraße 18, 5161Elixhausen, Austria
7 Laboratory ofZoology, Research Institute ofBiosciences,
University ofMons, Place du Parc 20, 7000Mons, Belgium
8 Swiss Ornithological Institute, Seerose 1, 6204Sempach,
Switzerland
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... This warming is harmful because it accelerates the metabolisms of ectothermic organisms and it also increases the activity of harmful fungi and parasites (Scharsack et al. 2021, Bertini et al. 2021 or impacts survival and fecundity in different taxa (Irwin andLee 2000, Williams et al. 2003), including cold-adapted bumblebees (Martinet et al. 2021, Ghisbain et al. 2023. These phenomena are often reflected by large population declines occurring in many species and, even more strikingly, by retreats towards the highest elevation, as for the case of orophylic bumblebees in the Alps and Pyrenees (Ornosa et al. 2017, Biella et al. 2017. Therefore, the spatial patterns of distribution changes due to climatic variations have the potential to diagnose the climatic sensitivity of biodiversity and warn towards a biodiversity-friendly management of cold areas (Brambilla et al. 2016(Brambilla et al. , 2017. ...
... Bumblebees are crucial high-altitude pollinators (Biella et al. 2021b). However, many bumblebee species are facing negative population trends, range contraction and altitude shifts with climate change considered one main cause among others (Kerr et al. 2015, Biella et al. 2017, Marshall et al. 2018. Moreover, laboratory tests indicated a high sensitivity to high and extreme temperatures (Oyen et al. 2016) and field observations detected body alterations due to heat islands in urban areas (Tommasi et al. 2022). ...
... Four species are particularly known for their link to cold areas and for their rarity: Bombus alpinus helleri , Bombus mendax ,Bombus mucidus and Bombus konradini . Bombus (Alpinobombus) alpinus (Linnaeus, 1758) has a disjoint distribution, as the subspecies alpinus occurs in the high Fennoscandia andhelleri occurs in the Alps at the highest elevation and formerly in the Carpathians, where it is now considered extinct (Rasmont et al. 2015, Biella et al. 2017. Bombus (Mendacibombus) mendax Gerstaecker, 1869 occurs at the highest elevation of the Alps with the subspecies mendax (Amiet et al. 2017) and of the Pyrenees with the subspecies latofasciatus Vogt 1909 (Ornosa et al. 2017), with a few more records on the Cantabrian mountains (Santamaría et al. 2011).Bombus (Mucidobombus) mucidus Gerstaecker, 1869 occupies the middle and high elevations of the Alps and of the Apennines (Manino et al. 2007), it occurs in the Pyrenees and it occurs also locally on the Cantabrian Range (Ornosa et al. 2017) and patchily in the Balkans and the Carpathians (Rasmont et al. 2015). ...
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Cold-adapted species endangered by global change are crucial cases for understanding range dynamics and its interface with conservation. In view of climate change and their sensitivity, Alpine insects should modify their distribution by reducing ranges, while being unable of sufficient displacements and mostly moving uphill. To test these hypotheses, we targeted four threatened, high-altitude bumblebees differing in subgenera and elevation ranges, and covering the main central and south European mountains. We performed species distribution models including climate and habitat, and we described elevation uphill and the year of change with broken-line regressions. Results indicate that climate change will cause severe future range contractions across large areas, more in the Apennines (80% - 85% ca) than the Alps and Pyrenees (24 - 56% ca), with mostly concentric retreats as future extents will nearly entirely be included in the present ones. Remarkably, since the ‘80s elevation uplift has started by about 325 - 535 m, a period coinciding with the beginning of the main warming, and will continue. The size and distribution of climate refugia will challenge conservation: they will be small and context specific (2-60% of current areas), but while in the Apennines and Pyrenees they will be nearly entirely within Protected Areas, only a third will be so for the Alps. Such impressive distribution changes demonstrates that cold-adapted bumblebees can accurately track climate change and be precise sentinels of it, and these results link with the investigated species being specialists with specific habitat requirements of temperature and glacier presence. Overall, the distribution of cold specialist bumblebees driven by climate change demonstrates that conservation should act upon the dynamic realities of species ranges because their range reduction, the impossibility of finding new areas and the movement uphill emerge as consistent patterns.
... Data fusion across remote sensing platforms with different spatial and spectral resolutions, coverage extents and collection frequencies can connect field surveys to landscape-level analyses (Alvarez-Vanhard et al., 2021). Unmanned aerial vehicles (UAVs) can effectively identify and monitor individual non-native species through targeted acquisitions of high-resolution imagery (Abeysinghe et al., 2019;Wijesingha et al., 2020). ...
... Preliminary modeling indicated that this proportion of background points, which are randomly selected across the prediction extent by MaxEnt, was needed to represent the range of conditions (Elith et al., 2011). We recorded permutation importance for each variable to evaluate which variables were most important for predicting clover (Phillips et al., 2021) and area under the receiver operating characteristic curves (AUC) for test data to evaluate prediction accuracy (Biella et al., 2017). Of the 11 alternative thresholds for classifying presences generated by MaxEnt, we used respective balance training omission, predicted area and threshold value (BTPT) values for both models as these aligned best with percent cover within UAV clover maps. ...
... Sentinel provides spatiotemporal coverage suitable to monitor landscape-level invasion dynamics (F€ orster et al., 2017;Kattenborn et al., 2019) provided that representative training data can aid classifications (Fassnacht et al., 2016). This can be facilitated through synergistic approaches that capitalize on complementary strengths across remote sensing platforms (Alvarez-Vanhard et al., 2021). Specifically, UAVs can capture continuous, high-resolution imagery to develop requisite training data of target species for classification of coarser resolution imagery (Gr€ anzig et al., 2021;Spence & Mengistu, 2016). ...
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... With climate change, bumble bee priority areas were identified in higher latitudes and in more mountainous regions, a pattern which has been observed previously (Biella et al., 2017;Kerr et al., 2015;Martins et al., 2015). Regions with overlap among conservation priority areas for each examined climate scenario (current, RCP 2.6 and RCP 8.5) may be especially important for conservation because they will provide suitable climate areas now and under multiple possible emission scenarios (Rose & Burton, 2009;Vos et al., 2008). ...
... This may be due to predicted patterns of climate change which are expected to cause the West Coast to become warmer and drier, potentially exceeding the thermal tolerances of bumble bees (Martinet et al., 2021) and limit food availability (Aldridge et al., 2011;Phillips et al., 2018). Additionally, montane bumble bee species would have restricted regions of suitability once they can no longer move to higher elevations or if alternate suitable mountainous regions are not within range (Biella et al., 2017;Inouye, 2020;Lee et al., 2019). However, eastern species or more distributed species may simply have more area to expand as the climate warms allowing for greater predicted gains without as many geographical barriers. ...
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... Other species occur only at high alpine elevations, such as B. alpinus, which may forage at ambient temperatures near freezing [27,31]. Accordingly, altitudinal range shifts caused by climate warming become threatening when species-specific pollen resources or host populations disappear, or when cold-adapted species cannot migrate to higher altitudes because they already inhabit the highest elevations [32,33]. Therefore, specialized bumblebee species and those with low dispersal abilities are more sensitive to climate change and rising temperature than widespread, generalist species [34,35] that find new pollen, nectar, and nesting sources more easily [36]. ...
... However, declines in bumblebee diversity have also been attributed to land use changes [17], particularly agricultural intensification [73,74]. Indeed, a loss of high-quality alpine pastures due to abandonment and usage competition with human activities such as skiing and a decline of grasslands due to construction activities can be observed in the study area [32,75]. This has also led to increasing scrub encroachment and more wooded areas. ...
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... Bumble bees are likely the best-studied group among insect pollinators in terms of their past and predicted future responses to increasing temperatures ( Jackson et al., 2022;Maebe et al., 2021;Soroye et al., 2020). Bumble bee communities are predicted to shift upward in elevation, with bees at the highest elevation unable to survive (Biella et al., 2017;Pradervand et al., 2014). Overall, climate warming is linked to predicted declines in the majority of bumble bee species, but a few species may benefit from warming temperatures ( Jackson et al., 2022;Soroye et al., 2020). ...
... In North America, bumble bees have high species richness in mountainous regions (e.g., Koch et al., 2015), facilitated by numerous thermal adaptations (Heinrich, 2004). The evolution of montane bumble bees has received increasing attention (Christmas et al., 2021;Jackson et al., 2018Jackson et al., , 2020Lee et al., 2019;Montero-Mendieta et al., 2019;Williams et al., 2015Williams et al., , 2018, driven by data demonstrating threats from climate change for these species (Biella et al., 2017;Marshall et al., 2020;Pradervand et al., 2014). ...
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Research Highlight: Ogilvie, J. E., & CaraDonna, P. J. (2022). The shifting importance of abiotic and biotic factors across the life cycles of wild pollinators. Journal of Animal Ecology, 91, 2412–2423. https://doi.org/10.1111/1365‐2656.13825. As global change and its multiple impacts continue to unfold across most of the planet, understanding how populations of wild species respond to changing conditions has become a major focus of ecological studies. Ogilvie and CaraDonna (Ogilvie & CaraDonna, 2022) focus on understanding how biotic and abiotic conditions affect bumblebee abundances. A major advance in their work is that, rather than focusing on a single measure of abundance at a particular life stage for each of the seven bumblebee species they survey (e.g. adult abundance), they focus on understanding the drivers of population abundance across the different stages of the species' life cycles. The authors specifically assess how three factors in particular, climate conditions, floral resource availability and previous life‐stage abundances impact these abundances. A main finding in their study is that each of these three factors directly impacted a different life stage, showing that just focusing on a single life‐stage would have resulted on a biased and incomplete picture of how abiotic and biotic factors affect bumblebee population dynamics. Studies like this one emphasize the need to focus on understanding the demographic mechanisms that determine population abundances. This Research Highlight assesses the work of Ogilvie & CaraDonna (2022), recently published in the journal, which focuses on the importance of considering multiple life stages when aiming at understanding the drivers of pollinator population abundances.
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Functions for species distribution modeling, calibration and evaluation, ensemble of models.
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