Bumblebee Diversity and Pollination Networks Along the Elevation Gradient of Mount Olympus, Greece

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Journal Article

Bumblebee diversity and pollination networks along the elevation gradient of Mount Olympus, Greece

Author(s): Minachilis, Konstantinos; Kantsa, Aphrodite; Devalez, Jelle; Trigas, Panayiotis; Tscheulin, Thomas; Petanidou, Theodora

Publication Date: 2020-11

Permanent Link: https://doi.org/10.3929/ethz-b-000440130

Originally published in: Diversity and Distributions 26(11), http://doi.org/10.1111/ddi.13138

Rights / License: Creative Commons Attribution 4.0 International

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Received: 28 January 2020 | Revised: 25 June 2020 | Accepted: 4 July 2020 DOI: 10.1111/ddi.13138

BIODIVERSITY RESEARCH

Bumblebee diversity and pollination networks along the elevation gradient of Mount Olympus, Greece

1Laboratory of Biogeography and Ecology, Department of Geography, University of the Abstract Aegean, Mytilene, Greece Aim: We studied bumblebee diversity and bumblebee pollination networks along the 2 Department of Environmental Systems altitudinal gradient of Mt. Olympus, a legendary mountain in Central Greece, also Science, ETH Zürich, Zürich, Switzerland 3Laboratory of Systematic Botany, Faculty known for its exceptional flora. of Crop Science, Agricultural University of Location: Mt. Olympus, Central Greece. Athens, Athens, Greece Taxon: Bombus (Latreille, 1802). Correspondence Methods: We explored 10 study sites located on the north-eastern slope of the Konstantinos Minachilis, Laboratory of Biogeography and Ecology, Department mountain, from 327 to 2,596 m a. s. l. Bumblebee surveys were carried out on a of Geography, University of the Aegean, monthly basis using pan traps (years 2013 and 2014) and random transect observa- Mytilene 81100, Greece. Email: [email protected] tions assisted by hand netting (years 2013, 2014, and 2016); visited flowering plants and their diversity were recorded during the transect observations. Funding information The research was partly co-financed by Results: With a total of 22 recorded bumblebee species and one species complex, Mt. the European Union (European Social Olympus is one of the richest mountains in Mediterranean Europe regarding bumble- Fund) and Greek national funds through the Operational Program “Education and bee diversity. Bombus quadricolor was recorded as a new species for Greece, whereas Lifelong Learning” of the National Strategic four species were recorded at their southernmost distribution limit, therefore pos- Reference Framework–Research Funding Program THALES, project POL-AEGIS (The sibly vulnerable to climate change. Species richness of both bumblebees and plants in pollinators of the Aegean: biodiversity and flower followed a unimodal pattern along the altitudinal gradient, the former peaking threats), Grant number MIS 376737. at high altitudes (1,900–2,200 m a.s.l.), the latter at lower to intermediate altitudes Editor: Markus Franzén (500–1,500 m a.s.l.). Bumblebee–plant visitation networks were larger, more diverse and more generalized in the between intermediate altitudes (1,500–1,800 m a.s.l.), while nestedness peaked at low and high altitudes. Main conclusions: Our results disclose the differential significance of the altitudinal zones of Mt. Olympus for the conservation of the diversity of bumblebees and their host plants, as well as of the interactions among them. Furthermore, they highlight the importance of this mountain, because of its South-European location, regarding climate change impacts on the bumblebee fauna of Europe. All in all, they point towards more reinforced conservation measures to be taken including the expansion of the protection status to the entire mountain.

KEYWORDS altitudinal gradient, Bumblebee diversity, global warming, Mount Olympus, mountain system, pollination network

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. © 2020 The Authors. Diversity and Distributions published by John Wiley & Sons Ltd.

.wileyonlinelibrary.com/journal/ddi Diversity and Distributions. 2020;26:1566–1581 | 1566 MINACHILIS et al. | 1567

1 | INTRODUCTION under different climatic scenarios (e.g. Kaloveloni, Tscheulin, Vujić, Radenković, & Petanidou, 2015). Mountain ecosystems constitute excellent model systems for test- Among all pollinator groups, bumblebees (Bombus Latreille ing physiological, ecological and evolutionary hypotheses within 1802) constitute a fundamental resource in mountain ecosystems. small spatial scales (Körner, 2000, 2003, 2007). Air temperature, This is mainly because they are cold-adapted, endothermic spe- atmospheric pressure and available land area decrease with alti- cies, remaining active in cool conditions when other pollinators tude, whereas solar radiation levels rise, resulting in increasingly are inactive (Heinrich, 1979). As a result, bumblebees are often the challenging abiotic conditions with far-reaching impacts on the most important pollinators in cool environments, such as the Arctic survival and reproduction of organisms, especially at the extremes (Løken, 1973), montane (Bingham & Orthner, 1998) and temperate (Körner, 2007). Studies performed along altitudinal gradients have (Ricketts et al., 2008) regions. Bumblebees are present at altitudes provided valuable insights on the effects of climate change on the di- even above 4,000 m a.s.l., providing invaluable pollination services versity and distribution of species, using space-for-time substitution to the alpine flora (Williams, 1991). A rise of the ambient tempera- scenarios (Mayor et al., 2017). There is little doubt that mountain ture may act against their adaptive advantage to exploit floral re- ecosystems should be placed under the spotlight, mainly because sources at higher altitudes by increasing competition with other the expected climatic changes in the 21st century are projected pollinators, with unknown consequences for the current species dis- to disrupt species distribution, with cascading effects on ecosys- tributions (Martinet et al., 2015). This is particularly likely in the east- tem services, such as pollination (Lefebvre, Villemant, Fontaine, & ern Mediterranean, because although it has long been considered a Daugeron, 2018; Rahbek et al., 2019). hotspot for wild bee diversity (Michener, 1979, 2000), the diversity Mediterranean mountains are of pivotal importance for biodi- of bumblebees is comparatively low (Balzan et al., 2016; Nielsen versity conservation, for two main reasons. First, because they are et al., 2011; Petanidou & Ellis, 1993; Varnava et al., 2020). Research key biogeographical elements in the Basin, having shaped species on bumblebee diversity in Mediterranean mountains is therefore distribution and diversity during glacial periods (Blondel, Aronson, paramount in order to assess the role of the genus in structuring Bodiou, & Boeuf, 2010). During the Pleistocene glacial periods, major mountain communities at different elevations and disclose the con- mountain ranges in the Iberian, Italian and Balkan peninsulas con- servational importance of these habitats for the genus. stituted refugia for northern species, which, during the subsequent Here, we study the patterns of diversity and pollination net- interglacial periods, including the Holocene, recolonized northern works of bumblebees along an altitudinal gradient of Mt. Olympus Europe (Hewitt, 1999). Consequently, temperate species constricted (2,918 m), a legendary landmark. The mountain constitutes a cir- their range to the southern peninsulas, to expand it later to northern cular massif of 25 km diameter on average, situated relatively near Europe or/and retreat to higher altitudes of Mediterranean moun- the central-east coast of Greece, and separated from other Balkan tains (Hewitt, 2011). Cold-adapted species, such as bumblebees mountains by plains, lower mountains and deep river valleys. Its (Hymenoptera: Apidae), expanded their range during the glacial pe- flora consists of >1,700 plant species, encompassing ca. 25% of the riods to the south and, in interglacial periods, returned to the north Greek flora, including 58 Greek endemics of which 25 are endemic or reached refugia at high mountain altitudes (Martinet et al., 2018; to Mt. Olympus itself (Strid, 1980; Strid & Tan, 1986, 1991). The Stewart, Lister, Barnes, & Dalen, 2010). It is well accepted that such mountain retained a certain level of glaciation in Pleistocene inter- climatic oscillations set the ideal conditions for population differen- glacial periods and even up to the Holocene (Smith, Damian Nance, tiation and speciation (especially in the refugia), and are responsible & Genes, 1997; Styllas et al., 2018), thus constituting a refuge for for the high levels of biodiversity and endemism in the Mediterranean glacial relics (Médail & Diadema, 2009), such as the local endemic Basin (Blondel et al., 2010; Hewitt, 2004). Jankaea heldreichii (Boiss.) Boiss. (Gesneriaceae) characterized as a The second reason why Mediterranean mountains are of piv- “living fossil” (Vokou, Petanidou, & Bellos, 1990). Because of its high otal importance for biodiversity conservation is because the altitude, the rich zonation along its elevation gradient, separation Mediterranean area is one of the most susceptible regions of the from other mountain ranges, high diversity of flora and fauna and world to climate change (Giorgi, 2006; Giorgi & Lionello, 2008). glacial history, Mt. Olympus is considered a model system for eco- Predictions suggest that over this century, widespread drought logical, evolutionary and biogeographical studies (Strid, 1980). High events will affect the Basin (Dai, 2012; Giorgi & Lionello, 2008), re- biodiversity and endemism suggest population differentiation and sulting in the highest desertification risk in the near future, world- speciation in past geological times when Mt. Olympus was a species wide (Hill, Stellmes, Udelhoven, Röder, & Sommer, 2008). In turn, refuge (Hewitt, 2004; Médail & Diadema, 2009). Until today, mainly it is expected that such a pronounced change in climatic conditions plant-focused studies have been conducted on the mountain, with at could affect the Mediterranean mountain systems more dramat- most partial consideration of plant–pollinator interactions, pollinator ically, and likely sooner, compared to montane systems of higher diversity, and community structure, and only at particular altitudes latitudes. Under this view, vital ecosystem services, such as pollina- (Blionis & Vokou, 2005 and references cited therein; Makrodimos, tion, should be thoroughly studied, both to cover knowledge gaps, Blionis, Krigas, & Vokou, 2008; Vokou et al., 1990). which are prominent in the region (Petanidou et al., 2013), and to be Pollination networks constitute a sophisticated tool to de- able to make projections for the future status of pollination services scribe and visualize the structure of interactions among plants and 1568 | MINACHILIS et al. pollinators within a community, allowing comparisons among com- (Figure 1). Along this route and at different altitudes and vegetation munities through specific metrics that can be computed. The tool has zones (see below), we established ten sampling sites with a NNE as- been employed to document such variation along altitudinal gradients pect, including both open areas and forest openings when inside a worldwide (Adedoja, Kehinde, & Samways, 2018; Cuartas-Hernandez forest; between successive sites, the average altitudinal difference & Medel, 2015; Hoiss, Krauss, & Steffan-Dewenter, 2015; Lara- was ca. 250 m and average distance in straight line ca. 1.5 km; in the Romero, Seguí, Pérez-Delgado, Nogales, & Traveset, 2019; Maglianesi, two cases the distance between sites was <1 km (in fact between Blüthgen, Böhning-Gaese, & Schleuning, 2015; Miller-Struttmann & 500 and 600 m), these sites were taken by necessity as the only ones Galen, 2014; Ramos-Jiliberto et al., 2010; Trøjelsgaard & Olesen, 2013), available (Figure 1, Table S1). Almost half of the mountain, specifically but only once within the wider Mediterranean area: Lara-Romero its eastern side, is part of the Olympus National Park, historically the et al. (2019) for Mt. Teide in Tenerife Island. The last study, however, first national park ever designated in Greece (1938), part of which was conducted only at four different high altitudes (between 2,350– constitutes a European Natura 2000 site (GR 1250001). Our study 3,520 m a.s.l.) and not at the entire altitudinal range of the mountain. sites cover all four major vegetation zones of Mt. Olympus, according In this study, we aim to explore the bumblebee patterns of diver- to Strid (1980): (a) evergreen–sclerophyllous (Mediterranean) scrub sity and function, that is involvement in pollination services within (300–600 m), (b) mixed beech and montane coniferous forests (700– communities occurring along the entire altitudinal gradient of Mt. 1,500 m), (c) cool temperate coniferous forests (1,500–2,500 m) and Olympus. This approach helps to disclose the present and histor- (d) alpine meadows (2,500–2,917 m). The climate is Mediterranean ical biogeography of the bumblebees in the Mediterranean, and at lower altitudes and temperate at intermediate to higher ones, with highlights conservation priorities regarding both species and habi- snow covering areas above 2,000 m from late October to late May tat types. It is noteworthy that among all studies investigating both (Strid, 1980). Afternoon thunderstorms are common in summer, and pollinator distribution/diversity and function along a mountain's alti- sudden snowstorms or hail may also occur. There is no permanent tudinal gradient, only two focused on bumblebees: Egawa and Itino water source above 1,100 m; thus, humidity from fog or low clouds (2019), who studied the elevation gradient 700–2,600 m a. s. l. of Mt. is of crucial importance. North-eastern slopes are more humid due Norikura, Japan; and Miller-Struttmann and Galen (2014), who ana- to their vicinity to the sea (Strid, 1980). lysed data from the Colorado Rocky Mountains collected by Macior (1974), limited, however, to only high altitudes, viz. >1,600 m a.s.l.. There are two additional studied areas of Mediterranean-type cli- 2.2 | Sampling of insects and their flowering mate, albeit focusing on all insect groups: Adedoja et al. (2018), a W. plant hosts Cape Province study, South Africa; and Lara-Romero et al. (2019), a study in the infra-Mediterranean/Canaries, limited to the highest al- Insect surveys were carried out within an area of ca. 0.1 ha at each titudes, >2,350 m a. s. l. Other studies focused solely on bumblebee site; they consisted of a collection of all insects using pan traps distribution along an altitudinal gradient, including Williams (1991) (years 2013 and 2014) and additional random transect observa- and Goulson, Lye, and Darvill (2008b) who studied Mt. Apharwat tions assisted by hand netting collection of unknown bumblebees (maximum study altitude 4,143 m, Kashmir) and Gorce and Tatra (years 2013, 2014 and 2016). Pan traps were placed as sets of three mountains (maximum study altitude 1,580 m, Poland), respectively. plastic bowls (triplets), each pan trap painted with a different UV- Our study is unique in that it explores bumblebee diversity patterns bright colour: blue, yellow and white (Nielsen et al., 2011; Westphal and involvement in pollination networks along the entire altitudinal et al., 2008). Triplets, five in each site and set at a distance of >5 m gradient of a mountain. from each other, were placed on height-adjustable metal stands in In particular, we address the following questions: order to be levelled with the height of the continuously growing vegetation during the sampling season, and thus being always visible to 1. How the composition and diversity of bumblebees and plants flying insects. Each pan trap was filled with a mixture of propylene vary along the altitudinal gradient of Mt. Olympus? glycol and water (1:1 in volume) and was left open to capture insects 2. Whether any bumblebee species are associated with specific alti- for a week. The use of propylene glycol was adopted for two rea- tudinal ranges? sons: to minimize evaporation and to preserve the collected speci- 3. Whether plant–bumblebee visitation network properties are alti- mens, thereby allowing a longer operational time of the pan traps. tude-dependent and how this varies along the gradient? Bumblebee surveys were carried out using hand netting in variable transect walks during which both bumblebees and the visited flowering plants were recorded (Nielsen et al., 2011; Westphal 2 | METHODS et al., 2008). Specimens of unknown bumblebees were collected together with the respective forage plants for later identification. 2.1 | Study area Hand netting lasted 90 min in 2013, and 120 min in the 2014 and 2016 surveys. The study was conducted on the north-eastern slope of Mt. Olympus, All insect observations and collections were carried out on a following the path route from Litochoro town to Mousses Plateau monthly basis from May to October of both 2013 and 2014 (both MINACHILIS et al. | 1569

FIGURE 1 Map showing the location of the study sites along the altitudinal gradient of Mt. Olympus, Greece (own spatial data depicted on Google Earth background) by pan trapping and hand netting), as well as of 2016 (only by hand (viz. different sampling methods and duration) were taken into ac- netting). Thus, the planning was to conduct a total of six sampling count in the analyses. Finally, because sites were selected not far rounds per year. Due to snow cover or harsh weather conditions in from the hiking path, carefully prepared bilingual informational signs certain years, a number of sites were inaccessible before June and were set to minimize disturbance by hikers. after September, resulting in fewer sampling rounds conducted All collected insect specimens were processed in the laboratory at these sites. They were the following: S-1838, S-1936, S-2262, and identified to species level, except for Bombus lucorum s.l., a com- S-2424 and S-2596 that were not sampled in 2013; and S-2262, plex consisting of three species that are indistinguishable with a mi- S-2424 and S-2596 not sampled in both 2014 and 2016. Yet, in croscope: B. lucorum, B. cryptarum and B. magnus; yet, because B. September 2014 pan traps at site S-2424 were destroyed by a terrestris was also difficult to distinguish under field conditions, visit heavy hailstorm. records of all the above species were pooled together as belonging The observation and collection of specimens was conducted in to the same group (Bossert, Gereben-Krenn, Neumayer, Schneller, days with fine weather favourable to bee activity and during the & Krenn, 2016; Wolf, Rohde, & Moritz, 2009). Bumblebee speci- active bumblebee foraging hours (10:00–16:00). During the survey, mens are kept at the Melissotheque of the Aegean (Laboratory of we tried to collect and observe bumblebees as thoroughly as pos- Biogeography and Ecology, Department of Geography, University of sible and to disturb them as little as possible. If occasional distur- the Aegean, Greece) (Petanidou et al., 2013). Voucher plant spec- bances may have occurred and some interactions missed, we trust imens are kept at the Herbarium of the Laboratory of Systematic this was evenly distributed over all sites along the altitudinal gra- Botany, Agricultural University of Athens, Greece. dient. As some bumblebee species are long-distance flyers, move- ment between sites could potentially have occurred, although we believe this was most unlikely to happen due to the topology and the 2.3 | Plant diversity and flower cover existing dense forests between sites. Several factors, like difficult accessibility (all sites above 1,200 m had to be accessed on foot), Number of plants in flower and their flower cover were measured accommodation restrictions (only one refuge along the path) and the within 1 × 1 m squares (n = 25) randomly selected at each site and erratic mountain weather, influenced the data collection, affected round (Lázaro, Tscheulin, Devalez, Nakas, & Petanidou, 2016). Flower both the choice of sampling methods and the sampling effort em- cover was measured by counting the number of flowers or inflores- ployed within a year (once per month) and in different years (vari- cences per plant species within the squares. Flower abundance for ation between years). To have comparable results, such differences each plant species was calculated as the average number of flowers/ 1570 | MINACHILIS et al. m2 per site. Specimens of plants that were difficult to identify on the 2.6 | Statistical analysis spot were collected for later identification. To test the relationship between altitude and bumblebee community composition, we used multivariate-response generalized linear 2.4 | Bumblebee diversity mixed models (MGLM) (R package mvabund 3.13.1). This approach fitted a separate GLM (binomial family with “cloglog” link) to the Using the combined pan trap and hand net data for the years 2013 distribution matrix of each insect of the network, using altitude as and 2014 separately, we computed three metrics that describe the explanatory variable, and a resampling-based hypothesis testing diversity of bumblebee species in the study communities: (Wang, Naumann, Wright, & Warton, 2012), and was used to indicate those species whose distribution showed a significant effect to (i) Species richness: the total number of species within a community. altitudinal change. The multidimensional response variable was the (ii) Shannon–Wiener diversity index (Hʹ): a widely used metric of α-di- presence/absence matrix of bumblebee species distribution among versity, which accounts both for the diversity and evenness of the ten sites, compiled by using the combined data from pan trap- species within a community. ping and hand netting of the years 2013 and 2014. The statistical (iii) Effective Number of Species (ENS): defined as the number of spe- significance of the fitted model was assessed with ANOVA (likeli- cies in a community with equal abundances that would give the hood ratio tests) using 999 bootstrap iterations via PIT-trap residual same as the observed value of α-diversity, and considered as the resampling. We used AIC to compare the best-fitted model with the true species diversity within a community (Jost, 2007). null model (y ~ 1). Univariate tests were subsequently performed to determine which response variables (bumblebee species) showed Metrics (ii) and (iii) were calculated using the R package vegan significant effects in response to altitude. 2.5-2. To test the relationship between altitude and the diversity of bumblebees on Mt. Olympus, we used Generalized Linear Mixed- effects Models (R package lme4 1.1-18-1) considering all pan trap- 2.5 | Network properties ping and hand netting data combined. To avoid pseudoreplication, we used “site ID” nested within “year” as categorical random vari- We calculated the following network properties, using all hand net- ables. As dependent variables, we used (i) the bumblebee spe- ting data recorded, each year considered separately (viz. years 2013, cies richness, (ii) the Shannon–Wiener diversity index and (iii) the 2014 and 2016), in order to describe the interacting bumblebees and Effective Number of Species (ENS), calculated for each of the sam- the plants observed to be visited by them in each of the ten commu- pled sites. For Shannon–Wiener index and ENS, we used models nities sampled (see Figures S1–S3). Namely, the following properties with Gaussian distribution, while for the bumblebee species rich- were calculated: ness, we used Poisson distribution and log link function (in the latter case, the model was not overdispersed; that is, the ratio between (i) Network size: the number of bumblebee–plant (b–p) links observed the residual deviance and residual degrees of freedom was <1.1 in each community. [Zuur, Ieno, Walker, Saveliev, & Smith, 2009]). As fixed variables (ii) Nestedness: the weighted NODF was used, which describes the (predictors), we included both the linear and the quadratic term of degree to which specialist species tend to interact with general- the altitude of each site. To avoid collinearity, we standardized the ist ones (Almeida-Neto & Ulrich, 2011). variable “altitude” (x = 0, σ = 1) before calculating its quadratic term. (iii) Linkage density: it represents the mean number of links per In addition, we used plant Shannon–Wiener index as a predictor. To species, weighted by the number of interactions (Bersier, select the best combination of predictors (including the interaction Banašek-Richter, & Cattin, 2002). Following (Lázaro, Tscheulin, terms of plant diversity and altitude), we used a backward selection Devalez, Nakas, Stefanaki, et al., 2016), we used this metric to process based on AICc (R package AICcmodavg 2.1-1). We also used estimate generalization, particularly where the networks dif- the ΔAICc in order to compare the best-fitted model with the null fered in size. model (y ~ 1). (iv) Shannon's diversity of interactions: the Shannon index calculated The same modelling approach (GLMMs) was used to test the for the different links of the network. relationship between altitude and species richness of the plants in

(v) Selectiveness: we used the H2ʹ index, which describes the selec- flower, “site ID” nested within “year” as categorical random vari- tiveness in the network, that is to which extent observed inter- ables, and the linear and the quadratic term of the altitude of each actions deviate from random selection of partners. The more site, as predictors. We used Poisson distribution and log link function

selective the species in the network, the higher the H2ʹ index (in the latter case, the model was not overdispersed; that is, the ratio (Blüthgen, Menzel, & Blüthgen, 2006). between the residual deviance to residual degrees of freedom was <1.1 [Zuur et al., 2009]). All the above metrics were calculated using the R package bipar- To test the relationship between altitude and the b–p visitation tite 2.11. network properties, we considered the hand netting data alone and MINACHILIS et al. | 1571

(a) Bombus mesomelas (b) Bombus niveatus (c) Bombus pratorum

e e

* ** *

Absence/Presenc

Absence/Presenc Absence/Presenc

Altitude (m) Altitude (m) Altitude (m)

(d) Bombus ruderarius (e) Bombus rupestris (f) Bombus soroeensis

* * *

Absence/Presence Absence/Presence Absence/Presence

Altitude (m) Altitude (m) Altitude (m)

(g) Bombus vestalis

* Absence/Presence

Altitude (m)

FIGURE 2 Bumblebee species occurrence along the altitudinal gradient of Mt. Olympus (based on data recorded in years 2013 and 2014 combined). Each panel shows the presence (value 1.0) or absence (value 0.0) of each of the seven bumblebee species associated significantly with specific altitudes along the gradient of the mountain. (*p ≤ .050; **p ≤ .010) applied GLMMs. To do so, we used the abovementioned network 3 | RESULTS properties (viz. network size, H2ʹ index, weighted NODF, linkage density and Shannon's diversity index) as dependent variables. As During the three study years, we recorded 5,255 bumblebees be- predictors, we used the linear and the standardized (see above) qua- longing to 22 species and one species complex (Table S2 in which dratic term of altitude, and flower abundance. As random factors, we species identification is of the lowest taxonomic level), which visited used site ID, nested within year (2013, 2014, 2016). We performed the flowers of 94 plant species (Table S3). analyses using (a) the Gaussian distribution for Shannon's diversity Bumblebee species occurrence on Mt. Olympus varied with alti- 2 and linkage density, (b) binomial distribution (link “logit”) for NODF tude (MGLM; ΔAIC = 36, χ = 104.4, p = .003; combined data of pan and H2ʹ, and (c) Poisson distribution for network size (link “log”) (the trapping and hand netting of the years 2013 and 2014). The distri- model was not overdispersed). To determine whether there was a bution of seven species correlated with altitude: Bombus mesomelas 2 2 significant altitudinal trend in the network properties, we used the (MGLM; χ = 8.6, p = .020), B. niveatus (MGLM; χ = 13.8, p = .005), 2 ΔAICc between the best-fitted model and the null model (y ~ 1). B. pratorum (MGLM; χ = 12.0, p = .011), B. ruderarius (MGLM; 1572 | MINACHILIS et al.

2 2 χ = 7.0, p = .025), B. rupestris (MGLM; χ = 12.0, p = .011), B. so- the lower sampling effort in 2013 (see Section 2), but also most likely 2 2 roeensis (MGLM; χ = 11.9, p = .011) and B. vestalis (MGLM; χ = 6.2, attributable to year-to-year significant variations occurring in nature p = .046). The specific altitudinal ranges these species are related (Petanidou, Kallimanis, Tzanopoulos, Sgardelis, & Pantis, 2008). with are shown in Figure 2. Plant species richness was highest at low to intermediate alti- Based on combined data (pan trapping and hand netting; sep- tudes, that is between 500 and 1,500 m in all three sampling years 2 arate sampling years 2013 and 2014), bumblebee diversity was (GLM; χ 2,4 = 13.6, p = .001) (Figure 4). Again, plant richness was low- found to be associated with high to very high altitudes (Figure 3a–c). est in 2013, probably due to the lower sampling effort in that year 2 Specifically, species richness peaked at 2,200 m (GLM; χ 2,4 = 13.3, (see Section 2). The bumblebee Shannon–Wiener index correlated p < .001), Shannon–Wiener at 1,900–2,000 m (LM; F1,14 = 80.4, with the plant Shannon–Wiener index (LM; F1,14 = 8.3, p = .012), and p < .0001) and ENS at 1,900–2,000 m (LM; F1,16 = 25.0, p < .0001). with the interaction between altitude and plant Shannon–Wiener

All diversity indices had higher values in 2014 vs. 2013, partly due to index (altitude × plant Shannon–Wiener: F1,14 = 6.7, p = .021).

(a) (b) 12 6 *** *** 10 5

8 4

6 3

2 4 2013 2013

Bumblebee species richness 2014 Effective Number of Species (ENS) 2014 1 2

300 600 900 1200 1500 1800 2100 2400 2700 300 600 900 1200 1500 1800 2100 2400 2700

Altitude (m) Altitude (m)

−0.01

−1e−05

−0.03

Bumblebee Shannon−Wiener −2e−05 2013 Bumblebee Shannon−Wiene −0.05 2013 2014 2014 −0.07 −3e−05

−0.10−0.05 0.00 0.05 0.10 −0.05 0.00 0.05 Altitude Plant Shannon−Wiener

FIGURE 3 Predictors of bumblebee diversity on Mt. Olympus. a–c: Altitude as predictor of bumblebee (a) species richness, (b) Effective Number of Species (ENS) and (c) Shannon–Wiener index; (d) Plant diversity as predictor of bumblebee diversity (viz. Plant Shannon–Wiener index vs. bumblebee Shannon–Wiener index). Plots (c) and (d) show the partial residuals of the best-fitted model that included both altitude and plant Shannon–Wiener index. The two fitted lines in each plot correspond to different sampling years, which represent random-effect factors in the fitted models (*p ≤ .050; ***p ≤ .001) MINACHILIS et al. | 1573

Interestingly, bumblebee diversity correlated negatively with plant species complex of bumblebees, consisting of three cryptic species. diversity (Figure 3d), probably as a result of the inverse diversity Such a rich bumblebee diversity is comparative with that recorded trends of the two groups along the altitudinal gradient (i.e., diver- in a much variable set of temperate habitats in NW Greece surveyed sity of plants peaked at lower to intermediate altitudes, while that of for a wider period of time, which encompassed a total of 29 species bumblebees at high ones [cf. above and Table S4]). out of the 33 currently known for Greece (Anagnostopoulos, 2005, The structure of b–p networks varied along the altitudinal gra- 2009, 2017; cf. Table 1). Mediterranean systems are notorious for dient for each of the three years of sampling (2013, 2014, 2016) their paucity in bumblebee diversity (Balzan et al., 2016; Nielsen (Figure 5). Networks were larger (i.e. included more links) be- et al., 2011; Petanidou & Ellis, 1993; Varnava et al., 2020) as com- 2 tween 1,500 and 1,800 m in all sampling years (GLM; χ 1,3 = 18.4, pared with temperate regions in the European continent (Table 1). p < .0001). (Note that 2013 networks were overall smaller than the Nonetheless, the Mediterranean mountains, characterized by mul- other two years, probably due to the lower sampling effort in that tiple climate zones and rich glacial history that favoured the pres- year; see Section 2). Linkage density also peaked at ca. 1,800 m (LM; ervation of bumblebee populations (Martinet et al., 2018; Médail &

F1,24 = 20.0, p < .0001); year 2014 did not follow this trend, proba- Diadema, 2009), host a high diversity of bumblebees as it is the case bly because metrics for the lowest altitude site (S-327) could not be of Susa Valley, Italy (Manino, Patetta, Boglietti, & Porporato, 2010), computed (only one bumblebee species was recorded, viz. B. terres- the French and Spanish sides of the Pyrenees (Iserbyt, 2009; Iserbyt, tris/lucorum s.l. group) (cf. Figure 5). Shannon's link diversity peaked Durieux, & Rasmont, 2008; Ornosa, Torres, & Rua, 2017) and the at around 1,800 m (LM; F1,24 = 13.5, p = .001). Finally, the b–p net- Cantabrian Mountains, Spain (Obeso, 1992; Ploquin, Herrera, & works were more nested at the extreme altitudes of the mountain, Obeso, 2013; Table 1). Mt. Etna, in Sicily, stands as an exception, that is <600 m and >2,400 m, showing an opposite trend than the with only 12 bumblebee species resulted, however, from a partly 2 other properties (GLM; χ 1,3 = 7.1, p = .008). The selectiveness index surveyed mountain just up to 1,900 m a.s.l. (Mazzeo, Bella, Seminara,

(H2ʹ) was found to correlate neither with altitude nor with flower & Longo, 2015). abundance. In fact, no property was correlated with flower abun- The present study discovered one new species for Greece, dance in the study sites: based on AICc, flower abundance was not viz. Bombus quadricolor which is a rare parasite specialist of B. so- included in any of the best-fitted models. roeensis. This parasitic species has a wide distribution range from the Cantabrian Mountains and the Pyrenees through to the Balkan mountains and Fennoscandia, with Mt. Olympus constituting its 4 | DISCUSSION southernmost distribution area (Rasmont et al., 2015). Furthermore, this study documented the range expansion of another three bum- 4.1 | Bumblebee diversity and faunistics blebee species, for which Mt. Olympus constitutes their southernmost distribution in Europe: B. monticola, whose range extends from Three years of systematic survey in ten sites along the altitudinal the Pyrenees to Fennoscandia, including the Alps and some Balkan gradient of Mt. Olympus yielded 22 identified species and one mountains (Martinet et al., 2018); B. hypnorum, a species with a wide distribution, from the Pyrenees and Balkan mountains in the south, to the Barents Sea in the north (Rasmont et al., 2015); and B. hae- *** maturus, a species that reaches Slovakia and Romania in the north 30 (Bossert & Schneller, 2014; Rasmont et al., 2015). Given their latitudinal restriction, the above four species can be considered as vulnerable to climate change, especially B. monticola being restricted to 25 the highest sites of Mt. Olympus (>2,400 m a.s.l., cf. Table S2) (Kerr et al., 2015; Rasmont et al., 2015). 20 Seven of the species of Mt. Olympus (B. mesomelas, B. niveatus, B. pratorum, B. ruderarius, B. rupestris, B. soroeensis and B. vestalis) 15 are significantly associated with specific altitudinal ranges on this Plant species richness mountain (Figure 2). This is in agreement with what is found in other

2013 mountains where bumblebee species have, however, much wider al- 10 2014 titudinal ranges than on Mt. Olympus (Figure 6). This might be the re- 2016 sult of (a) the non-sampling over all the sides of Mt. Olympus, (b) the 500 1000 1500 2000 2500 mostly non-systematic sampling approach of most previous studies Altitude (m) (usually done as entomological surveys), following a less strict place and time schedule (Table 1), (c) the limited altitudinal range of Mt. FIGURE 4 Altitude as predictor of plant species richness on Mt. Olympus as compared to other higher mountains and its low lati- Olympus. The three fitted lines correspond to different sampling years, which represent random-effect factors in the fitted models tude, and (d) climatological factors, for example the influence of the (***p ≤ .001) Atlantic to Cantabrian Mountains. 1574 | MINACHILIS et al.

(a) (b) 200 2013 *** 2013 ** 80 175 2014 2014

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FIGURE 5 Altitude dependence of the bumblebee–plant networks along the altitudinal gradient of Mt. Olympus. Scatter plots show altitude dependence of (a) network size, (b) nestedness, (c) Shannon's diversity of links and (d) linkage density. The fitted lines correspond to different sampling years, which represent random-effect factors in the fitted models (**p ≤ .010; ***p ≤ .001). The metrics for year 2014 could not be computed for site S-327 (cf. panels b, c, d) where only one bumblebee species was captured (viz. the group B. terrestris/lucorum s.l.)

Six of the above seven species (viz. B. mesomelas, B. pratorum, B. the least isolated, and certainly not fully isolated from the Balkan ruderarius, B. rupestris, B. soroeensis, B. vestalis) are associated to high mountain ranges, which explains not only the importance of this altitudes of Mt. Olympus (cf. Figure 2, Table S2 showing the abun- mountain as established species refuge but also why it constitutes dances of these species in different altitudes). Among all these spe- the southernmost distribution limit for the aforementioned bumble- cies, however, only B. mesomelas is exclusively associated with very bee species. high altitudes. Furthermore, as shown in Figure 6, our records of B. There is hard evidence on the decline of bumblebee spe- campestris signpost the highest altitudes this species has been ever cies worldwide (Cameron et al., 2011; Kosior et al., 2007) which recorded at. We have to emphasize the uniqueness of Mt. Olympus is associated not only with climate change, but also with land use by highlighting that, among the three mountains in Mediterranean change, pesticide use, pathogens, invasive species and combina- Europe close to the 40th parallel north with altitude ca. 3,000 m tions among these factors (Cameron & Sadd, 2020; Goulson, Lye, & a.s.l. (the others are Sierra Nevada and Mt. Etna), Mt. Olympus is Darvill, 2008a). Within the Olympus National Park protected area, MINACHILIS et al. | 1575

TABLE 1 Bumblebee species richness in different geographical entities and mountains of Europe

Study area Region # Species (km2) Study purpose Source

6 Entire Europe 68 10.4 × 10 Compilation of existing studies Nieto et al. (2014) UK (entire country) 22 242,495 Compilation of existing studies Goulson (2010) Florina District, Greece 29 1,924 5-year bumblebee survey, Anagnostopoulos (2005, 2009, 2017) 550–1,800 m a.s.l. Turkey (entire country) 47 783,562 Bumblebee survey, 0–3,500 m Rasmont, Aytekin, Kaftanoğlu, and a.s.l. Flagothier (2009) Susa Valley, Italy 30 1,261 10-year bumblebee survey, 124 Manino et al. (2010) locations, 340–3,130 m a.s.l. Mt. Etna, Sicily, Italy 12 581 10-year bumblebee survey, 9 Mazzeo et al. (2015) locations, 0–1,900 m a.s.l. Pyrenees, Eyne Valley, 33 21 5-year bumblebee survey, 457 Iserbyt et al. (2008) France locations, 1,450–2,850 m a.s.l. Pyrenees National Park, 30 2,521 3-year bumblebee survey, 703 Iserbyt (2009) France locations, 296–3,298 m a.s.l. Pyrenees, Spain 28 19,000 10-year bumblebee survey, 78 Ornosa et al. (2017) locations, 670–2,600 m a.s.l. Cantabrian Range, 28 10,600 2-year bumblebee survey, 80 Obeso (1992) Spain locations, 0–2,200 m a.s.l. Cantabrian Range, 21 10,600 3-year bumblebee survey, 53 Ploquin Spain locations, 0–2,200 m a.s.l. et al. (2013)

where this study was carried out, the most important threat bumble- glacial age. Unfortunately, past historical records of bumblebee dis- bees are likely to be impacted by in the near future is climate change. tribution are lacking, so no firm conclusion can be drowned at the And because climate change is considered as the main cause of moment. Theoretical models predict a severe reduction in suitable bumblebee decline by most recent studies (Kerr et al., 2015; Soroye, distribution area for most of the bumblebee species not only on Mt. Newbold, & Kerr, 2020), we justifiably expect the impact of climate Olympus but also for the entire Greece, as only four of the Greek change on Mt. Olympus to be significant. species are predicted to retain their present distribution (viz. B. argil- Communities are more vulnerable to loss of generalists, and laceus, B. niveatus, B. terrestris and B. vestalis: Rasmont et al., 2015). bumblebees are generalist pollinators offering pollination services Such predictions pinpoint towards the utter need of a regular bum- to numerous plant species (Memmott, Waser, & Price, 2004). This blebee monitoring scheme to track future changes in bumblebee dis- implies that the consequences in communities will be critical in tribution in the country, especially on Mt. Olympus. In this respect, case of bumblebee species extinction. We assume, however, global it is worth mentioning that of all species recorded on the mountain, warming effects to vary among communities along the altitudinal only one, B. laesus, has been included in the Red Data List under the gradient, not only because of the existence of microrefugia hosted status Near Threatened at European level (Nieto et al., 2014). within a highly heterogeneous microclimatic environment (Suggitt Our results indicate that the altitudes between 1,900 and et al., 2018), but also because of the communities’ diverse resilience 2,200 m a. s. l. are the most important for conserving the highest di- related to a variety of different factors. Such a factor, for instance, is versity of bumblebee species on Mt. Olympus. Such a predominance nestedness, which was found to increase community's resilience (the of high-elevational peak in bumblebee diversity agrees with other speed at which the community returns to the equilibrium following studies published so far. In some of them, bumblebee diversity was a disturbance) (Dalsgaard et al., 2013; Thébault & Fontaine, 2010), found to peak at relatively lower altitudes than on Mt. Olympus (at suggesting that in our case communities at low and high altitudes 900–1100 m, Gorce and Tatra mountains, maximum study altitude may be more resilient against global warming impacts (see pollina- 1,580 m high, Poland [Goulson et al., 2008b]; at 1,300–1,900 m, Mt. tion networks below). Norikura, maximum study altitude 2,600 m high, Japan [Egawa & Bumblebees respond to global warming by either restrict- Itino, 2019]). But Williams (1991) found bumblebee diversity to occur ing their southern (Kerr et al., 2015) or shifting uphill their lower even higher, between 3,000 and 3,800 m (Mt. Apharwat, maximum (Ploquin et al., 2013) distribution limits. Therefore, the observed study altitude 4,143 m, Kashmir). As it happens on Mt. Olympus, range expansion of bumblebees, both latitudinal (B. quadricolor, B. the diversity in alpine zone is generally lower than subalpine and monticola, B. hypnorum and B. haematurus) and altitudinal (B. camp- montane (cf. also Miller-Struttmann & Galen, 2014 exploring ele- estris), is either the result of a recent colonization due to present vations >1,600 m of the Colorado Rocky Mountains). These stud- climate change or these species have been established since the last ies on bumblebee diversity, however, were carried out at mountain 1576 | MINACHILIS et al.

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FIGURE 6 Bumblebee species distribution along the altitudinal gradient on Mt. Olympus (our data) and some other mountainous regions in Europe. The two horizontal lines indicate the altitudinal range (327–2,596 m) of our study on Mt. Olympus. Numbers in each species name refer to the following citations from which the data were obtained: 1. Anagnostopoulos (2005, 2009, 2017); 2. Iserbyt et al. (2008); 3. Manino et al. (2010); 4. Mazzeo et al. (2015); 5. Obeso (1992); 6. Ornosa et al. (2017); 7. Ploquin et al. (2013); and 8. Rasmont et al. (2009)

regions with different latitude, biogeography and geological history the last study also reports no significant altitudinal variation of than Mt. Olympus, so a comparison restricted to altitude is certainly butterflies on Rhodope Mountains. incomplete. As we already mentioned, the unique characteristics of Mt. Olympus establish the mountain as refuge and southernmost distribution limit for several bumblebee species, and this situation 4.2 | The host plants probably influences the altitudinal pattern of bumblebee diversity observed on the mountain. Plants displayed a low- to mid-elevational richness on Mt. Olympus, Studies looking at all pollinator species or different pollinator at much lower altitudes than bumblebees (500–1,500 vs. 1,900– guilds did not all come to the same conclusion as those focusing on 2,200 m, respectively; cf. Figure 4, Table S4). This implies that altitude bumblebees. Some found that, like in our case, insect pollinators functions as an ecological filter which is harsher to plants than it is displayed a hump-shaped relationship with altitude: Alps, Germany: to bumblebees, indicating that on Mt. Olympus the ecotone signify- Hoiss et al. (2015); Jonaskop Mountain, W. Cape Province, South ing the transition from woods to open alpine grasslands (coinciding, Africa: Adedoja et al. (2018); El Teide, Tenerife, Canary Islands: in fact, with the maximal bumblebee diversity) favours bumblebee Lara-Romero et al. (2019), presenting only data above 2,350 m. rather than plant diversity. This suggests that bumblebees’ ability to The results concerning Geometrid moths were similar (meta-anal- thermoregulate and the resulting advantages at higher altitudes, po- ysis on 26 global elevational gradients: Beck et al., 2017). On tentially leading to competitive release from other pollinator groups, the other hand, several studies found a clear linear decline with may outweigh the disadvantage of a decreased food-plant diversity. altitude not only for the entire pollinator group (Andes, Chile: Most of the studies on the diversity of host plants of all pol- Ramos-Jiliberto et al., 2010 based on data from Arroyo, Primack, & linators report a hump-shaped response of plants to elevation Armesto, 1982; Trøjelsgaard & Olesen, 2013, a meta-analysis using gradient, showing maxima at about the same or/and even higher 54 global data sets; Antioquia, Colombia: Cuartas-Hernandez & elevations (Adedoja et al., 2018; Hoiss et al., 2015) or at lower Medel, 2015), but also for bees (Alps, Germany: Hoiss, Krauss, elevations (Cuartas-Hernández & Gómez-Murillo, 2015; Lara- Potts, Roberts, & Steffan-Dewenter, 2012) and for butterflies Romero et al., 2019) as their visitors. Finally, two studies showed alone (Mt. Olympus, Greece: Kaltsas et al., 2018); interestingly, plant diversity to be altitude-independent: Egawa and Itino (2019); MINACHILIS et al. | 1577

Trøjelsgaard and Olesen (2013). To the above contrasting patterns, altitude (Ramos-Jiliberto et al., 2010) or to be altitude-independent it is interesting to add the only study reporting a continuous in- (Cuartas-Hernandez & Medel, 2015). crease of plant host diversity along the altitudinal gradient of the Network specialization (selectiveness index H2ʹ) did not correlate Rocky Mountains carried out by Miller-Struttmann and Galen with altitude in our study. In contrast, Hoiss et al. (2015) reported

(2014) that reported 8, 12 and 15 plant species interacting with decreased H2ʹ values with elevation, which agrees with Lara-Romero 19, 15 and 15 bumblebee species in montane, subalpine and alpine et al. (2019) who also found network specialization to decrease with zones, respectively. altitude. However, the results of both these studies are based on networks including all pollinator guilds. On the other hand, bumblebees are considered generalist pollinators (Goulson, 2010), consisting, 4.3 | Pollination networks however, of both long- and short-tongued species that both occur throughout the range of the mountain. As a result, b–p interaction We found bumblebee–plant interaction networks on Mt. Olympus networks are largely influenced by the differential bumblebee be- to be larger, more diverse, and more generalized at intermediate haviour, and the availability of floral resources that follows a some- altitudes (1,500–1,800 m), which is also reflected in the lowest what different altitudinal trend. All in all, we believe that the lack of nestedness values (NODF) found for the same altitudes (Figure 5, specialization trend along the altitudinal gradient of Mt. Olympus Table S5). This elevation range is higher than the range of plant di- versus other published studies may be the result of either having versity maxima (viz. 500–1,500 m) and lower than that of bumble- employed the full altitudinal range of Olympus versus a few sites bee diversity maxima (viz. 1,900–2,200 m) (cf. Figures 3a,b and 4; at particular altitudes (mainly the highest ones) employed in other Table S4). Evidently, the resulting larger, more diverse and more gen- studies, or because other studies present results of meta-analysis eralized b–p networks are encountered within the gradient where consisting of tens of different mountain studies in which particular- the highest diversity of both bumblebee and plant groups tends to ities are masked. overlap. This result highlights that the assessment of species diversity alone does not allow conclusions regarding the trends of interaction diversity (i.e., the diversity and architecture of plant–pollinator 5 | CONCLUSIONS interactions) along the altitudinal range of the mountain. To extend this thought, studies of biodiversity, along environmental gradients, We found bumblebee community structure on Mt Olympus to be should include not only the taxonomic, but also the interaction di- strongly altitude-dependent: (a) bumblebee species richness and versity, for example interspecific interactions, within the commu- diversity maximize at high altitudes; (b) bumblebee–plant networks nities (Kaiser-Bunbury & Blüthgen, 2015) in order to (a) elucidate are larger, more diverse and more generalized at intermediate alti- community biogeography, (b) predict responses to environmental tudes, whereas nestedness peaks at low and high altitudes; and (c) change and, ultimately, (c) help set solid and targeted conservation seven bumblebee species have a significant connection to certain objectives about for specific species or habitat types. altitudinal ranges. Nestedness (NODF), an indicator of asymmetry in b–p networks, Thus far, the conservation and protection measures applied in had its lowest values at intermediate altitudes on Mt. Olympus, the Olympus National Park (covering, however, only half the moun- where networks are larger (Figure 5b), implying that at the lower tain area) focus primarily on plants, birds and mammals. Our results and higher altitudes b–p networks consist of many specialist species provide evidence that conservation strategies should also include that are more likely to interact with generalist partners (Bascompte, pollinators, with emphasis on bumblebees, which represent major Jordano, Melián, & Olesen, 2003). The high nestedness value at the providers of pollination services, especially at higher altitudes. altitudinal extremities can be explained by the higher asymmetry Furthermore, our findings disclose the need to focus on multiple of b–p resources, as resulting from the low diversity ratio of bum- elevation zones regarding conservation priorities: high altitudes blebees:plants in the lower altitudes and the low diversity ratio of (1,900–2,200 m) harbour the richest bumblebee diversity; at lower to plants:bumblebees at higher altitudes (cf. Figure 3a–c, Table S4); intermediate altitudes (500–1,500 m), flowering plants display their this is corroborated by the low linkage density at either altitude highest diversity; and at intermediate altitudes (1,500–1,800 m), b–p (Figure 5d). In general, larger networks tend to have smaller values communities include the most diverse interactions. of nestedness (Kantsa et al., 2018; Trøjelsgaard & Olesen, 2013), Based on our results, we recommend the Olympus National Park which may also explain the observed trend at intermediate altitudes area should be extended to cover the entire mountain co-consid- where networks are the largest along the entire gradient. Like on Mt. ering all mountain sides and altitudes, and the conservation and Olympus, nestedness in b–p networks was found to increase at high protection schemes should comprehensively include measures elevations (Miller-Struttmann & Galen, 2014). Being the only studies against future threats to the bumblebee fauna, for example land focusing on b–p networks along an altitudinal gradient, their conver- use change and invasive species; authorities considerations to re- gent results imply that communities at high altitudes are more resil- duce the protected area to construct ski resort and the observed ient against global warming impacts (cf. above). However, in studies degradation of the non-protected area of the mountain justify our including all pollinators, nestedness was found to decrease with proposition as the only measure against human activities. Regular 1578 | MINACHILIS et al. monitoring, including especially pollination network properties and pollination services, should be established to track possible adverse Theodora Petanidou https://orcid.org/0000-0003-1883-0945 effects of climate change on communities along the altitudinal gradient and to allow for timely conservation actions (Kaiser-Bunbury REFERENCES & Blüthgen, 2015). For the time being, there are no local measures Adedoja, O. A., Kehinde, T., & Samways, M. J. (2018). Insect-flower inter- that could be effectively taken against the impact of global warming. action networks vary among endemic pollinator taxa over an elevation gradient. PLoS One, 13(11), e0207453. https://doi.org/10.1371/ Certainly, future research will fill this gap in order to advise us on the journal.pone.0207453 key species, specific measures and management schemes including Almeida-Neto, M., & Ulrich, W. (2011). A straightforward computational assisted migration, on Mt. 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