JHR 95: 231-244 (2023) ago Sy JOURNAL OF. teeters doi: 10.3897/jhr.95.87752 RESEARCH ARTICLE () Hymenopter a Q https://jhr.pensoft.net ‘The International Society of Hymenopteriss RESEARCH Niche modeling of bumble bee species (Hymenoptera, Apidae, Bombus) in Colombia reveals highly fragmented potential distribution for some species Laura Rojas-Arias', Daniel Gémez-Morales?, Stephanie Stiegel?, Rodulfo Ospina-Torres* | Biology Institute, Science Faculty, National Autonomous University of Mexico, University Avenue 3004, Mexico City México 2 Geography Department, Human Science Faculty, National University of Colombia, Carrera 45, Bogota, Colombia 3 Institute of Biology and Chemistry, University of Hildesheim, Universitatsplatz 1, Hildesheim, Germany 4 Laboratory of Bees Research, Biology Department, Science Faculty, National University of Colombia, Carrera 45, Bogotd, Colombia Corresponding author: Stephanie Stiegel (stiegel@uni-hildesheim.de) Academic editor: Christopher K. Starr | Received 14 June 2022 | Accepted 28 December 2022 | Published 17 February 2023 https://zoobank.ore!7 C72F539-B97F-4E66-BDD8-5AB0A37A12BF Citation: Rojas-Arias L, G6mez-Morales D, Stiegel S, Ospina-Torres R (2023) Niche modeling of bumble bee species (Hymenoptera, Apidae, Bombus) in Colombia reveals highly fragmented potential distribution for some species. Journal of Hymenoptera Research 95: 231-244. https://doi.org/10.3897/jhr.95.87752 Abstract Insect population decline has been reported worldwide, including those of pollinators important for eco- system services. Therefore, conservation actions which rely on available rigorous species distribution data are necessary to protect biodiversity. Niche modeling is an appropriate approach to distribution maps, but when it comes to bumble bees, few studies have been performed in South America. We modeled ecological niches of nine Colombian Bombus species with MAXENT 3.4 software using bioclimatic variables available from WorldClim. This resulted in maps for each species that show the potential distribution area at the pre- sent time. Modeled species maps accurately represent potential niches according to the description of bio- climatic conditions in the species’ habitat. We grouped the species into three clusters based on our results, as well as on distributional information from literature on the topic: High Mountain, Mid- Mountain and inter-Andean, and the Amazon and Eastern Plains Basin. Niche modeling depicted bumble bee species’ dis- tribution in Colombia, the results of which can serve as a useful tool for conservation policies in the country. Keywords biogeography, distribution, maxent, native bees, pollinators Copyright Laura Rojas-Arias et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 232 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) Introduction Bumble bee species (Bombus spp.) are one of the widest studied taxa of bees in the world and Colombia regarding their ecological traits, the genetic composition of populations, pathogens, and their role in pollination services (Cure and Rodriguez 2007; Gamboa et al. 2015; Jaramillo-Silva et al. 2018; Lotta-Arevalo et al. 2020). Buzz pollination carried out by bumble bees allows for the pollination of several crops of economic importance in Colombia, such as Solanaceae like potatoes, tomatoes, pa- prika, etc. (Cure and Rodriguez 2007; Riafo et al. 2015; Vinicius-Silva et al. 2017) or Passifloraceae like passion fruit, gulupa, curuba, etc. (Pinilla-Gallego et al. 2016). Also, bumble bees are important for the pollination of many plant species in natural ecosys- tems like paramos and cloud forests, which are key for water regulation in Colombia (Rubio 2012). For example, they serve in the pollination of several species of “frailejon” of the genus Espeletia (Fagua and Bonilla Gémez 2005). However, a drastic decline in insects has been documented worldwide (Hallmann et al. 2017; Seibold et al. 2019; Klink et al. 2020). A massive decline in the species dis- tribution of most bumble bees has been reported, especially in developed regions like Europe and North America (Goulson et al. 2008). In Europe, there have been reports of declines since the 50’s. Just in the United Kingdom, three species out of twenty-five have gone extinct, and eight report major declines (Goulson 2003). Similar results have been reported in North America. In Illinois alone, four species have become lo- cally extinct (Grixti et al. 2009). There is no population trend research of this kind performed in Colombia, and as one of the richest countries in terms of biodiversity (Rangel 2015), the country should increase research on its pollinators in order to de- velop preventive management of natural resources. Biogeographic information about species is vital for conservation planning. The study of species distribution patterns has two complementary approaches: historical biogeography, which elucidates the causal mechanisms of current distribution, and ecological biogeography, which evaluates the ecogeographic factors that are currently shaping the distribution of species, looking for patterns in characteristics that are re- quired for a species’ long-term survival. It looks at abiotic characteristics like humid- ity, temperature, or salinity and ecological characteristics like interactions with other organisms or genetical features. Research in this last approach is usually performed at a local scale a short time frame (Pérez-Malvaez and Gutiérrez 2003). Niche modeling is one of the methods used in ecological biogeography. It repre- sents the fundamental niche without considering the realized niche, which requires detailed field research and confirmed species samples. Niche modeling aims to find the potential distribution area of a species (Soberon and Miller 2009). It is important to have good quality and quantity of information for the models, as they can be biased if the data for a species is scarce. Thus, niche modeling can provide potential distribution maps for bumble bees in Colombia, updating and complementing the previous available maps, made by Abram- ovich et al. (2004). This information could be an important tool to use in both future studies with an evolutionary and ecological aim, as well as in conservation efforts by Niche modeling of Bumblebee species in Colombia p56} informing environmental conservation plans, political decisions, and public policies in Colombia, and by strengthening existing efforts like the Colombian Pollinators Initiative (CPI) (Nates-Parra 2016). As the importance of bee conservation continues to escalate, conservation actions are necessary to protect bees’ biodiversity (Sarospataki et al. 2005). Materials and methods Study area The geographical extent used for each species in the modeling process covers the entire continental Colombian territory, from the north (13°23.73'N) to the south (4°13.75'N) and from the west (81°44.13'W) to the east (66°50.63'W). No buffer was used. There are nine species from the genus Bombus reported for Colombia: B. pauloensis Friese, 1913 (formerly B. atratus Franklin, 1913), B. excellens Smith, 1879, B. funebris Smith, 1854, B. hortulanus Friese, 1904, B. melaleucus Handlirschi, 1888, B. pullatus Franklin, 1913, B. robustus Smith, 1854, B. rubicundus Smith, 1854, and B. transversalis Oliver, 1789. Across the paramo ecosystem, four species can be found with different altitudinal distributions: B. funebris between 2500 and 4750 m, B. hortulanus between 2100 and 3600 m, B. robustus between 2100 and 3800 m, and B. rubicundus between 2500 and 3900 m (Pinilla-Gallego et al. 2016). Along the sub-Andean forest or the cloud forest, two species can be found: B. excellens between 1500 and 2600 m and B. melaleucus between 450 and 2100 m. The most abundant species in the low moun- tain strata is B. pauloensis. However, it has a wide altitudinal range between 150 and 3600 m (Liévano et al. 1991). Finally, two different species can be found across tropical forests with warm and wet climates: B. pullatus between 120 and 3500 m (especially in the foothills) and B. transversalis between 180 and 1100 m (restricted to the amazon forest and its foothills). Occurrence data We obtained occurrence points from the Wild Bee Research Lab of the Universidad Na- cional de Colombia, Bogota (LABUN), the Insect Collection of Universidad del Quindio (CIUQ), the Francisco Luis Gallego Entomological Museum (MEFLG), Universidad Nacional de Colombia, Medellin, the Bee Collection of the Universidad Militar Nueva Granada, the Entomological Museum of the School of Agronomy at Universidad Na- cional de Colombia (UNAB), and the database from the Global Biodiversity Information Facility (GBIF). Occurrence points were adjusted using the altitude reference reported by Pinilla-Gallego et al. (2016). All occurrence point data were originally collected from 1938 until 2020, throughout different seasons and derived from various methods (See Suppl. material 1). The senior author checked all occurrence records to prevent recogniz- able errors in georeferencing and taxonomy. The number of points used for each specie was: B. excellens 46; B. funebris 150; B. hortulanus 1130; B. melaleucus 47; B. pauloensis 2128; B. pullatus 549; B. robustus 243; B. rubicundus 426; B. transversalis 43 (Fig. 1). 234 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) le opto . gee. j Ayacucho$ Sa | as ou val ' id > e- a 7 Species B. excellens B. rubicundus B. funebris B. pullatus + B. hortulanus B. pauloensis Patt o B. melaleucus B. transversalis ~ alee . } B. robustus Sources: Esri, HERE, Garmin, Intermap, inctement PC Corp., GEBCO,, USGS, | FAO, N NPS, NRCAN {GeoBase, IGN, Kadaster NL, Ordnance Survey, Esri I Fenon Japan, METI, Esri | China (Hong Kong), (c) OpenStreetMap contributors, and elas 14 Reserva the GIS User Community a ~~ Figure |. Distribution of the points used in the modeling of each specie. Niche modeling of Bumblebee species in Colombia 235 Environmental variables We used 19 environmental data layers for modeling (Table 1), which were downloaded from the WorldClim V. 2.1 website (Fick and Hijmans 2017). The layers represent the climate average from the year 1970 to the year 2000 at a spatial resolution of 30 Arc seconds (0.93 km”). Niche models QGIS 2.8 (QGIS Development Team 2016) was used to clip and convert environ- mental layers, enabling their use in MAXENT. Niche models were developed using MAXENT 3.4 (Phillips et al. 2020). Specific settings were set at the following defaults: a maximum of 500 iterations, 10% test point (CrossValidate), without extrapolation and cumulative, keeping a limit convergence of 0.00001 and prevalence of 0.5, maxi- mum number of background points 10000. Two different statistical analyses were performed per species: the Jackknife test to evaluate the weight or importance of each variable (Timana de la Flor and Romero 2015; Phillips and AT&T Research 2017), and the AUC (Area Under the Curve) test. Jack- knife test is a method for validating the samples and model. It shows the representative variables for modeling each specie (Shcheglovitova and Anderson 2013). According to the results of the Jackknife test, we selected the three variables with the highest percent- age of importance, whose values depend on each species. To obtain the AUC, the specific settings given above were chosen according to established knowledge about bumble bees’ altitudinal distribution (Pinilla-Gallego et al. 2016). Subsequently, an ROC (Receiver Operating Characteristics) curve was created, and the AUC was calculated. The AUC value reflects the model’s accuracy or its capacity for prediction. The AUC value moves between 0 and 1, with 1 representing a perfect prediction. Values over 0,9 are considered strong (Pliscoff and Fuentes-Castillo 2011). Finally, ArcMap 10.5 (ESRI 2015) was used for reclassifying and visually representing the ecological niche modeling results. Table |. Bioclimatic variables included in modeling were obtained from WorldClim. Temperature Precipitation 1 Annual Mean Temperature 12 Annual Precipitation 2 Mean Diurnal Range (Mean of monthly (max. temp.-min. temp.)) 13 Precipitation of Wettest Month 3 Isothermality (BIO2/BIO7) (x100) 14 Precipitation of Driest Month 4 Temperature Seasonality (standard deviation x 100) 15 Precipitation Seasonality (Coefficient of Variation) 5 Max. temperature of Warmest Month 16 Precipitation of Wettest Quarter 6 Min. Temperature of Coldest Month 17 Precipitation of Driest Quarter 7 Temperature Annual Range (5-6) 18 Precipitation of Warmest Quarter 8 Mean Temperature of Wettest Quarter 19 Precipitation of Coldest Quarter 9 Mean Temperature of Driest Quarter 10 Mean Temperature of Warmest Quarter 11 Mean Temperature of Coldest Quarter 236 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) Results The models showed good results for all nine bumble bee species, with AUC values above 0.9, although the number of occurrences for Bombus excellens, Bombus melaleucus, and Bombus transversalis was low. Bombus pauloensis and Bombus hortulanus had the highest number of occurrences, being common in collections (Table 2). Based on our results and distributional information from scientific literature, we divided the bumble bee species into three distributional groups: high mountain bumble bees, mid-mountain/ inter-andean bumble bees, and Amazon and eastern Plains basin bumble bees. High Mountain bumble bees The potential distribution areas for B. funebris, B. hortulanus, B. robustus, and B. rubicundus occurred only in high mountain departments, along a range of different small and fragmented areas, with a high probability of occurrence in the central part of the Eastern Andes Range (Fig. 2). B. funebris represented the most restricted and fragmented species. B. hortulanus occurrences had the lowest altitudinal points for this group. B. robustus data was similar to B. hortulanus but included some areas in the northern part of the Eastern and the Central Ranges. B. rubicundus showed similar potential distribution to B. robustus but with more restricted and fragmented areas. Mid-Mountain and Inter-Andean bumble bees This group of species showed a wider altitudinal and potential distribution than the high mountain species, along and between the three mountain ranges (Fig. 3). B. excellens showed a higher probability along most of the Central and Eastern moun- tain ranges, as well as in the mid-mountain area of the Sierra Nevada de Santa Marta. For B. melaleucus, its potential distribution was indicated along the three moun- tain ranges. B. pauloensis exhibited a continuous distribution over the Andean region. B. pullatus was concentrated along low altitudinal areas of the inter-Andean valleys. Table 2. Bumble bee species data for the area under the curve (AUC obtained by niche modeling), num- ber of occurrences used for modeling, and the distributional group selected for each species according to our results and previous results by Pinilla-Gallego et al. (2016). Species AUC 1970-2000 Distributional group Bombus excellens 0.951 Mid-mountain and inter-Andean Bombus funebris 0.976 High Mountain Bombus hortulanus 0.977 High Mountain Bombus melaleucus 0.965 Mid-mountain and Inter-Andean Bombus pauloensis 0.911 Mid-mountain and Inter-Andean Bombus pullatus 0.917 Mid-mountain and Inter-Andean Bombus robustus 0.983 High Mountain Bombus rubicundus 0.973 High Mountain Bombus transversalis 0.999 Amazon and Eastern Plains Basin Niche modeling of Bumblebee species in Colombia 237 QWQLOMBIA | Z L ; , ea Eee on LOMBIA © sma i \ ‘i \ 4 j ry J LR, ies { rea a : iA Vey foes Quite “ieee enta = 7 y Cu ered 4 \ Cu eweda . a abil aie hal nats aa nau \ 4 waa 4 pres ne FCUADOR 7 ECUADOR: N Ht Ten y 4 y ra = “0! 70 140 280 Km Loreto 0 70 140 280 Km RETO ptr eas \ Py i Bs _ AMA?ON a er ee pli AMA? ON Geer d * J ie Can oo valencia Marcy Z f, Barquisimeto Seon ‘Barquisimeto Toe ‘: sage fee Eaton nyo es y a ~ i pao > \ r 4 r - ) pe } / { \ . " roo abe Quevedo “4 mesa Cf ous hah - r ™ o ha idee |. BGUADOR N BGUADOR N Hutte “0. 70 140 280 Km 7 ee “0 70 140 280 Km ORETO f f Fy — "4 AMAZON Ay a " P aa AMAZON _ W a bbe va “ec at ey ; F - 4 ay i f is a f an \ a f a \ P [ fe oe dt cits! date Re | Hg { cae va on Sait rh isn Legend Probability of occurrence |__| None [7] Low {__| Medium [J High Figure 2. Potential distribution maps for High Mountain bumble bees A B. funebris B B. hortulanus C B. robustus D B. rubicundus. 238 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) raw c. Caracas re] Caw MF valendi Maracey fl Barquisimeto a Tere dl Ca Baoime A ac. AMG? in| 6 || i ee ab: Ain 5 nts — wW oma 5» \ i Se Pe i Pe et a ey lO CR \ ~ ; \ a u Nim \ { pci \ Ree cemetary Neon a ie Gee | RN ee "sae cabal Baal N 280 Km LORETO pera Seas Py sels pried ae ar AMAZON - Pe Taal M re cna Raa . j sources: Esri, Ojeda Chane Kio oh lid ee ka ae WOLOMBIA = 4 fee LOMBIA = _- i ee oo ce a eo a ee LP 8 el” | a amis santa nepans ™ : Mate et an Noma baie |» ECUADOR nN ECUADOR Pe mes ee Hates i Hates “0, 70 140 280 Km LORETO = Femi: WA ene “0. 70 140 280 Km LORETO. oe Finite hs rie f he Pa ya vs AMAZON =) cere. ay “ waAZON J LF, Pune? ure J LF, (Mf oa f _ agin, a ~ Mee fre! ety oa eo a rage ~ a — [~ s y orm f a é y corned = if same ad Ps meer ody sama ad . [ Zi Pj Sourons: Est, USGS, NOAA; Sources: Es, Gamin, USGS, NPS lg i i Sources: Est, USGS, NOAA; Sources: Es", Garmin, USGS, NPS Legend Probability of occurrence |__| None [7] Low {__| Medium [9 High Figure 3. Potential distribution maps for Mid-Mountain and Inter-Andean bumble bees. A B. excellens B B melaleucus C B. pauloensis D B. pullatus. Niche modeling of Bumblebee species in Colombia 239 Amazon and Eastern Plains Basin bumble bees Bombus transversalis is the only species with a potential distribution along the Ama- zon Forest, the Andean foothills, and the Orinoquia region. The eastern part of Meta presented the highest altitudinal points for the species at 1150 m. The northern area of the biogeographic region of Chocé showed optimal bioclimatic conditions for B. transversalis, but no occurrence point was found or used there for this model (Fig. 4). The variables with the highest weight for each species are presented in Table 3. San “cable Carga Felipe Nalenaa Siareeky Barquisimeto ee i : “Sane Acarigua Castos Montelibano “~Caveast ip.” jartadé f =Medeltin quill ECUADOR .~ Tofantins Santo Anténio do Ica Fi “0 70 140 280 Km LORETO ft. etida rs t pe ge er — e a Carauari mee J ? Laan Sources: Esri, USGS, NOAA; Sources: Esri, Garmin, USGS, NPS. Legend Probability of occurrence |__| None [7] Low |_| Medium [J High Figure 4. Potential distribution map for Amazon and Eastern Plains Basin bumble bees, B. transversalis. 240 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) Table 3. Bioclimatic variables had the highest weight in the model for each species, according to the results obtained by the Jackknife test. Species (Distributional group) Variables with the highest weight (Percent of contribution) 1 7nd 3M Bombus excellens (Mid- 8. Mean Temperature of 1. Annual Mean Temperature 6. Min. Temperature of Coldest Mountain and inter-Andean) Wettest Quarter 94.35% 94.27% Month 94.04% Bombus funebris 4. Temperature Seasonality 6. Min. Temperature of Coldest 1. Annual Mean Temperature (High Mountain) 95.50% Month 94.54% 94.03% Bombus hortulanus 11. Mean Temperature of 1. Annual Mean Temperature 10. Mean Temperature of (High Mountain) Coldest Quarter 96.72% 96.63% Warmest Quarter 96.61% Bombus melaleucus (Mid- 5. Max. Temperature of 11. Mean Temperature of 1. Annual Mean Temperature Mountain and inter-Andean) Warmest Month 95.20% Coldest Quarter 95.16% 95.14% Bombus pauloensis 6. Min. Temperature of Coldest | 11. Mean Temperature of 8. Mean Temperature of (High Mountain) Month 91.30% Coldest Quarter 91.18% Wettest Quarter 91.09% Bombus pullatus (Mid- 11. Mean Temperature of 8. Mean Temperature of 4. Temperature Seasonality Mountain and inter-Andean) Coldest Quarter 83.91% Wettest Quarter 83.53% 76.67% Bombus robustus 5. Max. Temperature of 6. Min. Temperature of Coldest 8. Mean Temperature of (High Mountain) Warmest Month 93.74% Month 93.72% Wettest Quarter 93.51% Bombus rubicundus 6. Min. Temperature of Coldest 1. Annual Mean Temperature 8. Mean Temperature of (High Mountain) Month 96.70% 96.70% Wettest Quarter 96.48% Bombus transversalis (Amazon 13. Precipitation of Wettest 11. Mean Temperature of 6. Min. Temperature of Coldest and Eastern Plains Basin) Month 98.88% Coldest Quarter 97.87% Month 96.94% Discussion These potential distribution maps for bumble bees in Colombia improve the previous maps available (Abrahamovich et al. 2004) for the species, with more precise areas of potential distribution and a visual schema for patterns already described in the litera- ture (Pinilla-Gallego et al. 2016). The four high-mountain species are associated with the paramo and high Ande- an ecosystems (Pinilla-Gallego et al. 2016). Paramo ecosystems are characterized as biogeographical islands, highly isolated areas with a great deal of endemism and low genetic flow between populations (Lotta-Arevalo et al. 2020). As a result, the poten- tial distribution of these species is highly fragmented. B. excellens, B. melaleucus, and B. pullatus are associated with mountain forests, and it is remarkable that, even though they showed a wide suitable area (Fig. 3A, B, D, respectively), there is a low number of occurrences. This indicates a small population size and high vulnerability. For example, B. excellens can only be found in the cloud forest, an ecosystem with an accelerated rate of deforestation (Nates-Parra 2006). B. pauloensis (Fig. 3C) shows a wide altitudinal and potential distribution consistent with its high plasticity in the habitat chosen for nesting (Liévano et al. 1991; Nates-Parra et al. 2006), and this is reflected by its wide distribution along the mountain areas. Its potential distribution will help conservation planning, as B. pauloensis positively impacts national agricultural productivity by pol- linating staple foods such as fruits and vegetables (Cure and Rodriguez 2007; Riafo et al. 2015; Poveda et al. 2018) due to its adaptability to disturbed habitats. According to its biogeographical history, for B. transversalis the Andes Mountain Range repre- sents a physical barrier for emigration. Thus, the potential distribution area in the biogeographical region of Chocé is not likely (Abrahamovich et al. 2004). The eastern Niche modeling of Bumblebee species in Colombia 241 area of Meta stands out as an expansion of previously recorded areas to include the low areas of the Andean foothills. The most important bioclimatic variables for bumble bees in Colombia are related to temperature (Table 3). Thus, drastic temperature changes put bumble bees in a condition vulnerable to threat under a climate change scenario (Gonzalez et al. 2021). Also, the potential distribution for most species overlaps with densely populated areas. Therefore, these maps are a tool for the detailed location of bumblebee biodiversity for conservation planning as bumble bee’ populations and their associated services will probably soon be reduced (Williams and Osborne 2009; Pinilla-Gallego et al. 2016). Conclusion The potential distribution for Colombian bumble bee species is reported here. Seven of them show a restricted distribution, shaped mainly by temperature restrictions. These results are a direct contribution to knowledge about Colombian bumble bee species, constituting useful knowledge for conservation, territorial planning, protection plans, and environmental management. Thus, by obtaining the most suitable areas for a spe- cies, this study can provide the ideal location to breed and reproduce the native species. These species contribute to improving the agricultural productivity of several regions by pollination. Likewise, this information can help avoid the introduction of foreign species for this purpose (Nates-Parra 2016). It is necessary to increase research efforts on bees for them to be included in conservation planning. Acknowledgements We would like to thank M. Sc. Andrea Lorena Garcia and M. Sc. Daniela Hoyos- Benjumea from the Insect collection at Universidad del Quindio, Ph.D. Diego Ria- ho from the bee collection in Universidad Militar Nueva Granada, Ph.D. Francisco Serna from the entomological museum Universidad Nacional, School of Agronomy, Bogota, and Ph.D. Sergio Orduz and biol. Carlos Londofo from the entomological museum Francisco Luis Gallego for their contributions to occurrence data. We are indebted to Ph.D. Sydney A. Cameron for comments and suggestions that improved this manuscript. We acknowledge financial support by Stiftung Universitat Hildesheim. References Abrahamovich AH, Diaz NB, Morrone JJ (2004) Distributional patterns of the Neotropical and Andean species of the genus Bombus (Hymenoptera: Apidae). Acta zoolégica mexicana 20: 99-117. https://doi.org/10.21829/azm.2004.2012002 GBIF (2021) Global Biodiversity Information Facility. https://www.gbif-org/ [April 18, 2021] 242 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) Cure JR, Rodriguez D (2007) Efecto de Bombus atratus (Hymenoptera: Apidae) sobre la pro- ductividad de tomate (Lycopersicon esculentum Mill.) bajo invernadero en la Sabana de Bogota, Colombia. Agronomia Colombiana 25: 62-72. https://repository.agrosavia.co/ handle/20.500.12324/980 ESRI (2015) ArcGIS ArcMap 10.5. Fagua JC, Bonilla Gdmez MA (2005) Ecologia de la polinizacién de Espeletia grandiflora en el Parque Chingaza. In: Estrategias adaptativas de plantas del paramo y del bosque altoandino en la Cordillera Oriental de Colombia. Universidad Nacional de Colombia. https://reposi- torio.unal.edu.co/handle/unal/53365 Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302-4315. https://doi. org/10.1002/joc.5086 Gamboa V, Ravoet J, Brunain M, Smagghe G, Meeus I, Figueroa J, Riaflo D, de Graaf DC (2015) Bee pathogens found in Bombus atratus from Colombia: A case study. Journal of Invertebrate Pathology 129: 36-39. https://doi.org/10.1016/j.jip.2015.05.013 Gonzalez V, Cobos ME, Jaramillo-Silva J, Ospina-Torres R (2021) Climate change will reduce the potential distribution ranges of Colombia's most valuable pollinators. Perspectives in Ecology and Conservation 19(2): 195-206. https://doi.org/10.1016/j.pecon.2021.02.010 Goulson D (2003) Bumblebees: Their Behaviour and Ecology. Oxford University Press, 260 pp. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annual Review of Entomology 53: 191-208. https://doi.org/10.1146/annurev.ento.53.103106.093454 Grixti JC, Wong LI, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biological Conservation 142: 75-84. https://doi.org/10.1016/j. biocon.2008.09.027 Jaramillo-Silva J, Ospina-Torres R, Henao-Cardenas MM, Rodriguez A, Parra G (2018) Passion fruit in Colombia. In: The pollination of cultivated plants. A compendium for practition- ers. Balboa, Ancon, Republic of Panama, 226-232. Liévano A, Ospina-Torres R, Nates-Parra G (1991) Distribucién altitudinal del género Bombus en Colombia (Hymenoptera: Apidae). Trianea 4: 541-550. Lotta-Arevalo I, Vargas-Ramirez M, Parra G, Matta N, Ospina-Torres R (2020) Accediendo al pasado: uso de especimenes de coleccién como fuentes de informacién genética para el género Bombus (Hymenoptera: Apidae). Revista de Biologia tropical 68: 394-414. https:// doi.org/10.15517/rbt.v68i2.36350 Nates-Parra G [Ed.] (2016) Iniciativa colombiana de polinizadores: Abejas ICPA. In: Iniciativa co- lombiana de polinizadores. Departamento de Biologia, Universidad Nacional de Colombia, Bogota D.C., Colombia, 42 pp. http://localhost:8080/handle/1 1438/8800 [April 16, 2021] Nates-Parra G (2006) Abejas corbiculadas de Colombia. Hymenoptera: Apidae. Unimedios - UN Periddico, 152 pp. http://historico.unperiodico.unal.edu.co/ediciones/90/13_b.htm [October 12, 2021] Nates-Parra G, Parra A, Rodriguez A, Baquero P, Vélez D (2006) Abejas silvestres (Hymenop- tera: Apoidea) en ecosistemas urbanos: Estudio en la ciudad de Bogota y sus alrededores. 1: 77-84. https://doi.org/10.25100/socolen.v32i1.9369 Niche modeling of Bumblebee species in Colombia 243 Pérez-Malvdez C, Gutiérrez RR (2003) Las ideas biogeograficas y su presencia en una revista mexicana: La Naturaleza. Llull: Revista de la Sociedad Espafiola de Historia de las Ciencias y de las Técnicas 26: 207-244. Phillips SJ, AT&T Research (2017) A brief tutorial on Maxent., 1-39. Phillips SJ, Dudik M, Schapire RE (2020) Maxent software for modeling species niches and distributions (Version 3.4.1). https://biodiversityinformatics.amnh.org/open_source/ maxent/ Pinilla-Gallego M, Ospina-Torres R, Cure J (2016) Bombus, los abejorros de paramo. In: Ini- ciativa Colombiana de Polinizadores. Capitulo Abejas. 129-142. http://investigacion.uni- tropico.edu.co/wp-content/uploads/2016/08/Abejas. pdf Pliscoff P, Fuentes-Castillo T (2011) Modelacion de la distribucidn de especies y ecosistemas en el tiempo y en el espacio: una revisién de las nuevas herramientas y enfoques disponi- bles. Revista de Geografia Norte Grande 48: 61-79. https://doi.org/10.4067/S07 18- 34022011000100005 Poveda CA, Riafio Jimenez D, Aguilar Benavides L, Cure JR (2018) Eficiencia de polinizacién de colonias huerfanas de Bombus atratus (Hymenoptera: Apidae) en fresa (Fragaria x ananassa) bajo cubierta. Acta Bioldgica Colombiana 23: 73-79. https://doi.org/10.15446/abc. v23n1.61648 QGIS Development Team (2016) QGIS Geographic information system 2.8.9. Open Source Geospatial Foundation Project. Rangel O (2015) La biodiversidad de Colombia: significado y distribucién regional. Revista de la Academia Colombiana de Ciencias Exactas, Fisicas y Naturales 39: 176-200. https:// doi.org/10.15446/abc.v23n1.61648 Riano D, Pacateque J, Cure JR, Rodriguez D (2015) Pollination behavior and efficiency of Bombus atratus Franklin in sweet peppers (Capsicum annum L.) grown in a greenhouse. Revista Colombiana de Ciencias Horticolas 9: 259-267. https://doi.org/10.17584/ rcch.2015v9i2.4182 Rubio Fernandez D (2012) Disponibilidad, uso y preferencia por los recursos florales en una comunidad de abejorros (Hymenoptera: Apidae: Bombus) en el paramo de Chingaza. Universidad Nacional de Colombia. https://repositorio.unal.edu.co/handle/unal/10829 [March 16, 2021] Soberon J, Miller C (2009) Evolucién de los nichos ecolégicos. Miscelanea Matematica 49: 83-99. https://doi.org/10.1016/s0186-1042(13)71195-1 Timana de la Flor M, Romero MAC (2015) Biogeografia predictiva: técnicas de modelamiento de distribucién de especies y su aplicacién en el impacto del cambio climatico. Espacio y Desarrollo: 159-179. https://doi.org/10.18800/espacioydesarrollo.201501.008 Vinicius-Silva R, Parma D de F, Tostes RB, Arruda VM, Werneck M do V (2017) Importance of bees in pollination of Solanum lycopersicum L. (Solanaceae) in open-field of the South- east of Minas Gerais State, Brazil. Instituto de Botanica. https://doaj.org/article/ae03d- £3e10504786bbb7bacf66ec056e [November 12, 2022] Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40: 367-387. https://doi.org/10.1051/apido/2009025 244 Laura Rojas-Arias et al. / Journal of Hymenoptera Research 95: 231-244 (2023) Supplementary material | Points used for the Niche modeling of Bumblebee species (Hymenoptera, Apidae, Bombus) in Colombia Authors: Laura Rojas-Arias, Daniel Gémez-Morales, Stephanie Stiegel, Rodulfo Ospina- Torres Data type: COL (excel document). Explanation note: Ocurrence data used for the modeling. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODDbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/jhr.95.87752.suppl1