ORIGINAL PAPER

The effect of fire history in shaping diversity patternsof flower-visiting insects in post-fire Mediterranean pineforests

Maria Lazarina1,2 • Stefanos P. Sgardelis2 • Thomas Tscheulin1 •

Jelle Devalez1 • Vangelis Mizerakis1 • Athanasios S. Kallimanis2 •

Spyridon Papakonstantinou1,3 • Thanassis Kyriazis1 •

Theodora Petanidou1

Received: 23 December 2015 / Revised: 21 September 2016 / Accepted: 30 September 2016� Springer Science+Business Media Dordrecht 2016

Abstract Fire affects diversity and structure of flower-visitor communities.We explored the

effect of fire history on the diversity patterns and structure of the flower-visitor guilds (bees,

beetles, flies, sawflies, and wasps), across a post-fire regeneration sequence of pine forests in

Rhodes Island, Greece. Fire history was defined by fire frequency and post-fire age of sites.

We did not find significant differences in species richness and abundance per guild between

fire-history regimes except for the abundance of flies, sawflies and the entire flower-visitor

community. Fire strongly affected the community structure of bees, beetles, and sawflies.

Communicated by B. D. Hoffmann.

This article belongs to the Topical Collection: Forest and plantation biodiversity.

Electronic supplementary material The online version of this article (doi:10.1007/s10531-016-1228-1)contains supplementary material, which is available to authorized users.

& Maria Lazarinamlazarin@bio.auth.gr

Stefanos P. Sgardelissgardeli@bio.auth.gr

Thomas Tscheulint.tscheulin@geo.aegean.gr

Jelle Devalezjdeval@geo.aegean.gr

Vangelis Mizerakisenv10057@env.aegean.gr

Athanasios S. Kallimaniskalliman@bio.auth.gr

Spyridon Papakonstantinous.papakonstantinou@apdaigaiou.gov.gr

Thanassis Kyriaziskiriazis83@hotmail.com

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Biodivers ConservDOI 10.1007/s10531-016-1228-1

Some of the most abundant and common species responded significantly to fire in terms of

abundance; yet, we observed no significant variation in the abundance of the common species

of bees, the most prominent pollinator group, implying that provision of pollination services

may not be considerably affected by fire. Long-unburnt sites displayed higher heterogeneity

in species composition compared to recently-burnt sites (either burnt once or twice). This

pattern deviated significantly from null expectations when analyzing the abundance-based

metric of b-diversity and was obscure in the case of the presence/absence-based metric,

indicating that fire affected mainly the spatial distribution of individuals, i.e. themain change

is not due to species turnover but to changes in relative abundance. Furthermore, the species

composition in recently-burnt sites (burnt once in 2008)weremore similar than in twice-burnt

sites (including areas burnt once between 1984 and 1992, and in 2008), indicating that fire

frequency affected post-fire heterogeneity of species composition.

Keywords Bees � Beetles � Flies � Generalized Linear Models � b-diversity �Null modelling

Introduction

Flower-visiting insects provide critical ecosystem services for both wild plant communities

and crops. Their multifaceted ecological role includes pest control and pollination,

although not all flower visitors are pollinators. Globally, insect pollinators are responsible

for the sexual reproduction of 88 % of angiosperms (Ollerton et al. 2011). In addition,

more than 70 % of the major food crops are either pollinator-dependent or at least profit

from animal pollination (Klein et al. 2007). However, these insects are impacted by

multiple human-induced disturbances resulting in their decline worldwide (Biesmeijer

et al. 2006). The main drivers of this global decline are climate change, land use change,

habitat loss and fragmentation, agricultural intensification, invasive species, and pathogens

(for a review see Potts et al. 2010).

Fire is a frequent disturbance and is considered an integral natural characteristic of

Mediterranean-type ecosystems (for a review see Pausas et al. 2008). Mediterranean pine-

woodlands are among the most fire-sensitive ecosystems as their post-fire regeneration is

hindered by increased frequency, intensity, and severity of fires (Pausas et al. 2008;

Koutsias et al. 2012). Forest fires affect vegetation dynamics and ecosystem processes,

resulting in a mosaic of different habitats and various initial post-fire communities (Elia

et al. 2012). Thus, fire shapes abundance and structure of post-fire insect communities

indirectly through changes in vegetation and soil, but also directly through mortality by fire

(Moretti et al. 2006). The post-fire succession of insects depends on the characteristics of

post-fire vegetation and surrounding habitat, the availability of resources, i.e. food and

Theodora Petanidout.petanidou@aegean.gr

1 Laboratory of Biogeography and Ecology, Department of Geography, University of the Aegean,81100 Mytilene, Greece

2 Department of Ecology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece

3 Dodecanese Forest Directorate, G. Mavrou 2, 85132 Rhodes, Greece

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nesting sites, and the insects’ ability to exploit them, as well as on insects’ recolonization

abilities (Swengel 2001; Potts et al. 2003, 2005; Moretti et al. 2006). As an immediate

effect of fire, diversity decreases due to direct mortality and starvation because of limited

food resources (Ne’eman et al. 2000). Local and regional diversity, as well as abundance

tend to increase during the first post-fire years as the dominating annual plants provide a

wide range of food resources, and the increased availability of bare ground and dead wood

offer them a wealth of nesting opportunities (Potts et al. 2003, 2005). Several studies,

however, found no significant difference in species richness and/or abundance of flower-

visiting insects after fire (Moretti et al. 2006; Elia et al. 2012; Cruz-Sanchez et al. 2014;

Rubene et al. 2015), while others report negative effects of fire, e.g. the destruction of

certain types of nesting sites (Winfree et al. 2009).

Variation in species composition (b-diversity) describes the relationship between

regional and local diversity, and may capture underlying ecological processes and the way

local changes scale up to regional diversity. Therefore, b-diversity is a key concept for

understanding the effects of disturbance on communities (Myers et al. 2013) and is

important for monitoring and conservation of regional diversity (Socolar et al. 2016).

Disturbance, such as fire, can result in increased (Hawkins et al. 2015) or decreased b-diversity (Chase 2007) by changing the community assembly processes or through

stochastic effects (Myers et al. 2013, 2015). One hypothesis posits that fire changes the

underlying community assembly processes; i.e. fire acts as environmental filter resulting in

homogenization of species composition in the disturbed habitats, thus lowering b-diversity.A null modelling approach estimating the deviation of b-diversity from expectations under

random assembly processes, i.e. controlling for differences in community size or in species

abundances, can help understand whether observed patterns of b-diversity is the product of

randomness or of fire-induced environmental filtering.

In an earlier study we found that bee responses to fire are mediated by functional traits.

This suggests that the structure of bee communities across fire-history regimes are affected

by species traits (Lazarina et al. 2016). In this study, using the same set of burnt areas, we

examine the effects of fire history (defined by post-fire age and fire frequency) on species

richness, abundance, community structure, and b-diversity of the entire flower-visitor

community. Specifically, we address the following questions: (1) Do a-diversity (species

richness at the site level) and abundance vary across different fire-history regimes? (2) Are

there differences in community structure across fire-history regimes? If yes, which species

respond significantly to fire history in terms of abundance? (3) Does fire result in lower

variation of species composition (lower b-diversity, i.e. biotic homogenization)?

Adversely, are the observed patterns within the randomly expected range?

Materials and methods

Study system and site selection

The study region of 373 km2 is situated in south-central Rhodes, southeastern Aegean,

Greece. The climate is Mediterranean with long hot summers and mild winters. The mean

annual temperature in the region ranges from 16.4 to 18.6 �C, and annual precipitation

from 828 to 910 mm (data from WorldClim, Hijmans et al. 2005).

The major fire events in the region during the last 50 years occurred in 1984, 1987,

1988, 1989, 1992, and 2008 all between June and September. As a result, the vegetation of

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the region is a mosaic of different-age scrub mixed with mature pine forests (Pinus brutia).

With the help of aerial photographs and ground-truth inspections, we selected 28 sites, with

distances between sites ranging from 0.37 to 25.43 km (mean distance = 8.21 km) (Fig. 1)

and assigned them to fire-history regimes according to fire history defined by post-fire age

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and fire frequency (Table 1): (1) unburnt for at least the last 50 years (UB, 4 sites, min

distance = 3.77 km, max distance = 25.43 km, mean distance = 14.70 km); (2) old-

burnt (OB, 6 sites, min distance = 1.23 km, max distance = 15.31 km, mean dis-

tance = 9.57 km) including areas which had a single fire between 1984 and 1992; (3)

twice-burnt (TB, 9 sites, min distance = 0.37 km, max distance = 12.36 km, mean dis-

tance = 6.10 km) including twice-burnt areas, once between 1984 and 1992 and once in

2008; (4) recently-burnt (RB, 9 sites, min distance = 0.59 km, max distance = 12.15 km,

mean distance = 4.82 km) including areas burnt once, in 2008. As preliminary statistical

analyses showed no significant differences in abundance and diversity between OB and UB

sites, these sites were considered as one group (named as long-unburnt sites, hereafter

referred to as LUB); distance between LUB sites ranged from 1.23 to 25.43 km (mean

distance = 12.34 km). This reclassification also facilitated statistical analyses as it led to a

more even distribution of sites in all fire-history categories. The study sites were dominated

by different entomophilous plants, such as Cistus creticus, C. salviifolius, Calicotome

villosa, Genista acanthoclada, Thymbra capitata, and Lavandula stoechas, with their

mixture varying among sites.

Sampling

Sampling of the flower-visiting insects was carried out in spring 2012 by employing the

common passive method of UV-bright pantraps (Westphal et al. 2008). In each site, five

triplets, each containing three UV-bright pantraps of yellow, blue and white colour, were

placed with 15 m minimum distance between each triplet. Each pantrap was filled with ca.

350 ml of water and a drop of dish washing detergent to break the surface tension and left

bFig. 1 Geographical distribution of the 28 sampled sites in the study region situated in south and centralRhodes Island, Greece, showing wild fire occurrences during the last 50 years. The sites were assigned tofour fire-history regimes according to their fire history defined on the basis of post-fire age and frequency offire: (i) unburnt for at least the last 50 years (UB, 4 sites); (ii) old-burnt (OB, 6 sites) including areas whichhad a single fire between 1984 and 1992; (iii) twice-burnt (TB, 9 sites) including twice-burnt areas, oncebetween 1984 and 1992 and once in 2008; (iv) recently-burnt (RB, 9 sites) including areas burnt once, in2008. Please note that UB and OB sites are considered as one group (LUB = long-unburnt sites) in all theanalyses. The a-diversity was the number of species at each sampled site. The b-diversity was analyzed ineach fire regime as the mean dissimilarity in species composition of sites within each regime. Also for eachfire regime we calculated the regional species richness as the total number of species in all sites of eachregime

Table 1 Number of sampling sites (n) in the study area across different fire-history regimes defined by firehistory, i.e. time since last fire (post-fire age), and fire frequency. Based on preliminary statistical analysesthat showed no significant differences between sites burnt once 20–28 years earlier (OB) and unburnt sitesfor at least the last 50 years (UB), these sites were considered as one group (LUB = long-unburnt sites) in allthe analyses

Fire-history regime Abbreviation n = 28 Post-fire age (years) Fire frequency

Twice-burnt TB 9 4 2

Recently-burnt RB 9 4 1

Long-unburnt LUB 10 [20 0

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collecting for 48 h. Three surveys were conducted per site at one-month intervals between

late March and late May 2012.

Flower-visiting insect groups

From all insect guilds collected in the pantraps we selected for the analysis those we know

from experience that are actual flower-visitors, albeit of variable pollination efficiency:

bees (Apoidea), beetles (Coleoptera), flies (Diptera), sawflies (Symphyta), and wasps

(Aculeata). Among flies (Diptera), we considered only the two major anthophilous fami-

lies, bee flies (Bombyliidae) and hoverflies (Syrphidae). The butterflies (Lepidoptera) were

excluded from our analysis, due to the low numbers in our samples. The collected insects

were identified to species level by specialists and deposited in the ‘‘Melissotheque of the

Aegean’’ (Petanidou et al. 2013), an entomological collection of ca. 200,000 specimens

from the Aegean established at the Laboratory of Biogeography and Ecology, University of

the Aegean.

Statistical analysis

Fire effects on species diversity and abundance

We summed the abundances of bees, beetles, flies, sawflies, and wasps across pantrap

triplets and surveys of the entire season. The abundance and richness of each site, as well

as total and mean values per fire-history regime were calculated for the entire flower-visitor

community and for each guild separately. The a-diversity corresponds to richness per site.

We explored the effect of fire-history regime on abundance and richness using Generalized

Linear Mixed Model approach, with fire history as fixed-effect variable and site as cate-

gorical random variable to avoid pseudoreplication. We calculated both the number of

species unique to one fire-history regime and those common across all regimes.

Fire effects on community structure

To explore how community structure differs among fire-history regimes, we constructed

multivariate Generalized Linear Models (hereafter GLM) with the function manyglm of the

package mvabund (Wang et al. 2012). For each flower-visitor guild, we fitted a GLM

model to the abundances using Negative Binomial error distribution to account for

overdispersion of data. As explanatory variables we used fire history and the first Spatial

Filter estimated by the ‘‘Spatial Analysis in Macroecology’’, SAM version 4.0 (Rangel

et al. 2010), to account for spatial autocorrelation. Pairwise comparisons were made by

repeating the main test using each fire-history regime as the reference group. Post-hoc tests

in the main GLM model were performed to explore the univariate responses of individual

species i.e. to determine which species significantly respond to fire-history, in terms of

abundance. The significance of explanatory variables was tested with the anova.manyglm

function (log-likelihood ratio statistic method LR, 500 permutations).

Fire effects on b-diversity

For each flower-visitor guild and for the entire flower-visitor community, b-diversity was

quantified by the index N* (Lazarina et al. 2013) at community level. The index N* is

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defined as the average sampling effort at which the total number of shared species

occurrences becomes equal to species richness. The index was estimated as the intersection

point between the line y = (a/2)n and S(n), where a is the average a-diversity, n the

number of samples and S(n) the average species accumulation curve. N* index does not

depend on a-diversity and sampling effort and reflects the heterogeneity of species com-

position. We used the R functions provided by Lazarina et al. (2013).

We explored the effect of fire history on b-diversity under the hypothesis that fire acts asenvironmental filter resulting in homogenization of the community. Within each fire-

history regime, we calculated the b-diversity values across sites. Then, we compared these

values across regimes. Our hypothesis was that the species composition among long-

unburnt sites would be more dissimilar (higher b-diversity) than among recently-burnt sites

(either once or twice-burnt). We calculated presence/absence-based Jaccard and abun-

dance-based Bray-Curtis pairwise dissimilarity indices. Then, we formulated a GLM

(Gaussian error distribution and identity link function) predicting each b-diversity index as

function of fire history and of distance separating the sites to account for spatial auto-

correlation. Distance was modeled by natural splines with two degrees of freedom i.e.

nonparametric smoothing functions to account for non-linear relationships. Fire history

was defined by a three-level factor, expressing the fire-history regime to which each paired-

dissimilarity value corresponded: within recently-burnt (RB), within twice-burnt (TB),

within long-unburnt sites (LUB).

To identify patterns of beta diversity and underlying community assembly processes, we

estimated the deviation of observed b-diversity values from null expectations (hereafter b-deviations), following Tucker et al. (2015). The observed values of Jaccard dissimilarity

index were compared to the distribution of null model expectations of randomly shuffled

species to sites according to their among-site occupancy i.e. controlling for differences in

community size and a-diversity. The observed values of Bray-Curtis dissimilarity index

were compared to the distribution of null model expectations of randomly shuffled indi-

viduals according to their among-site frequency, i.e. controlling for spatial aggregation of

individuals (random sampling effects). The null models were constructed for each fire-

history regime, i.e. we treated each regime as a different community, for each flower-

visitor guild and for the flower visitors in total. The b-deviations were estimated by the R

functions provided in the supplementary material of Tucker et al. (2015). Then, we for-

mulated a GLM predicting b-deviations as a function of distance and of fire history as in

the case of observed values of b-diversity.All analyses were performed using R version 3.1.0 (R Development Core Team 2014).

Results

Fire effects on species diversity and abundance

In total, 6341 insect individuals were collected. Online Resource 1 provides a summary of

the abundance and species richness of each insect family collected. The flower-visiting

insects belonged to 220 species, of which 100 species were bees (1707 individuals), 48

beetles (3648 individuals), 10 flies (only hoverflies and bee flies were included: 66 indi-

viduals), 6 sawflies (524 individuals), and 56 wasps (396 individuals). Within each guild,

the most abundant species were: the beetle Tropinota hirta (1571 individuals), the bee

Lasioglossum malachurum (1023 individuals), the sawfly Macrophya postica (508

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individuals), the wasp Chrysis ignicollis (74 individuals), and the bee fly Lomatia polyzona

(28 individuals). The mean values and standard deviation of abundance and species

richness of each fire-history regime for the entire flower-visiting community and for each

guild are presented in Online Resource 2. According to Generalized Linear Mixed Model

analysis, fire history had a significant effect on the abundance of flies, sawflies and of the

entire flower-visiting community, with recently-burnt sites exhibiting significantly higher

abundances than all remaining regimes However, no significant effect of fire history was

detected on the abundance of bees, beetles and wasps (Online Resource 3). Fire history had

no significant effect on richness of the entire flower-visitor community and of any flower-

visitor guild (Online Resource 4). The highest numbers of unique flower visitors, mainly

bees and wasps, occurred in the long-unburnt sites, whereas the lowest numbers in the

twice-burnt sites (Fig. 2). The pattern was similar across all flower-visitor guilds except for

flies and sawflies (Online Resource 5 presents a list of the species present in only one fire-

history regime). Among all guilds, beetles displayed a high proportion of species present in

all fire-history regimes, a fact that is well reflected in the lowest b-diversity detected

(N* = 3.80). Bees exhibited the highest b-diversity (N* = 9.03), followed by wasps

(N* = 8.30), flies (N* = 4.90), and sawflies (N* = 3.92). The N* value of the entire

flower-visitor community was 6.29.

Fire effects on community structure

The multivariate GLM analysis showed that fire history and the spatial component sig-

nificantly affected the structure of the entire flower-visitor community, bee community and

Fig. 2 Venn diagram showing the number of species of each fire-history regime and shared number ofspecies between fire-history regimes for the entire flower-visitor community (a) and for each guild (b–f).Fire-history regime abbreviations: TB = twice-burnt sites, RB = recently-burnt sites, LUB = long-unburntsites (old-burnt and unburnt sites)

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beetle community (Table 2). Fire history significantly affected the sawfly community,

while no significant effect was detected in flies and wasps (Table 2). The structure of the

entire flower-visitor community and that of the beetles differed significantly among fire-

history regimes. The bee community of twice-burnt sites differed significantly from long-

unburnt sites. Finally, the sawfly community of recently-burnt sites differed significantly

from all other regimes. The univariate analysis for species demonstrated that 13 species

(five bee, seven beetle, and one sawfly species) responded significantly to fire history in

terms of abundance. The bee species with significant response to fire history (Andrena

limata, A. morio, A. tomora, Eucera cypria, Halictus sexcinctus) were locally rare species

(i.e. with low local abundance); the beetle species with significant response to fire history

(Online Resource 6) included four abundant species, Trichodes punctatus, Acmaeoderella

villosula, Anthaxia sp. 8 and Cryptocephalus rugicollis, with the latter three species more

abundant in recently-burnt sites and also three species locally rare (Anthaxia sp.1, Bli-

topertha lineolata, Stenopterus rufus). Among sawflies, the very abundant Macrophya

postica responded significantly to fire history and was more abundant in recently-burnt

sites (once burnt).

Table 2 Significant pairwise differences in community structure in terms of abundance across fire-historyregimes as estimated by multivariate generalized linear models (repetition of the main test using each timedifferent fire-history regime as reference group). We also give the p-value of fire history as defined inTable 1 and of spatial component expressed by the first ‘‘Spatial Filter’’ as estimated by the ‘‘SpatialAnalysis in Macroecology’’ (SAM, version 4.0). The analyses were performed for the entire flower-visitorcommunity and also for each guild (bees, beetles, flies, sawflies, and wasps). The significance was calculatedusing ANOVA in multivariate GLMs (by log-likelihood ratio statistic, 500 permutations)

Deviance p value Main effects GLM Pairwise comparisons

F-statistic p value

Flower-visitor community

Fire history 649.90 0.004 22.11 0.005 TB = RB = LUB

Spatial filter 392.80 0.002

Bees

Fire history 260.70 0.04 13.26 0.005 TB = LUB

Spatial filter 190.10 0.005

Beetles

Fire history 193.30 0.002 13.80 0.005 TB = RB = LUB

Spatial filter 103.10 0.002

Flies

Fire history ns ns ns

Spatial filter ns ns

Sawflies

Fire history 24.85 0.024 5.104 0.015 RB = {TB, LUB}

Spatial filter 5.52 0.503

Wasps

Fire history ns ns ns

Spatial filter ns ns

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Fire effects on b-diversity

The GLM analysis showed that fire history had a significant effect on presence/absence

dissimilarity in the entire flower-visitor community and for each flower-visitor group

(p\ 0.05), while distance had no significant effect except in sawflies. In all cases, within

regime mean dissimilarity was higher in long-unburnt sites, except for flies where twice-

burnt sites exhibited the highest dissimilarity (Fig. 3d). Specifically, bee, wasp, and entire

flower-visitor community dissimilarity was significantly higher in long-unburnt sites ver-

sus once or twice recently-burnt sites (Fig. 3a, b, f). The beetle and sawfly dissimilarity

was significantly lower in recently-burnt sites (Fig. 3c, e). A similar, but stronger pattern

was observed when considering abundance-based dissimilarity, with long-unburnt sites

showing significantly higher dissimilarity than recently-burnt sites (once or twice) in all

guilds (Fig. 4a–c, e, f) but flies (Fig. 4d). Distance had a significant effect on bee, wasp and

sawfly abundance-based dissimilarity index. Furthermore, within regime, dissimilarity

based on presence/absence and abundance metrics was higher in twice-burnt sites than in

recently-burnt sites for most guilds. For the presence/absence-based metric, a higher dis-

similarity was found in twice-burnt sites versus recently-burnt sites for beetles, sawflies,

and flies. For the abundance-based metric, the pattern was more prominent, with all guilds

(except bees) having significantly higher dissimilarity in twice-burnt sites versus recently-

burnt sites.

Fig. 3 Mean effect plots of presence/absence-based within fire-history regime dissimilarity estimated byJaccard index (mean ± standard error) as a function of fire-history regime showing the results of formulatedGeneralized linear models predicting within fire-history regime dissimilarity as a function of distancebetween sites and fire history for (a) flower-visitor community, and for each guild (b–f). Different lettersindicate significant differences between fire-history regimes, according to GLM analysis. Fire-historyregime abbreviations: TB = twice-burnt sites, RB = recently-burnt sites, LUB = long-unburnt sites (old-burntand unburnt sites)

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The presence/absence b-deviations were very low for the entire flower-visitor com-

munity, the bees, and the wasps across all fire-history regimes (Fig. 5a, b, f), suggesting

that their species composition did not differ from the null model (random assembly)

expectations. Fire history and distance had no significant effect on the presence/absence

b-deviations of the entire flower-visitor community, of bees, and of wasps. In all other

cases, fire-history and distance had significant effects on presence/absence b-deviations.The beetles and sawflies demonstrated negative b-deviations, with twice-burnt and long-

unburnt being close to zero and recently-burnt sites significantly lower (Fig. 5c, e). For

flies b-deviation in twice-burnt sites was positive and significantly higher than in other

regimes which had negative values (Fig. 5d). Regarding abundance-based b-deviation,fire-history regime had a significant effect in all cases, while the effect of distance was

not significant. The flower-visitor community, the bees and sawflies showed the highest

mean values of b-deviations in the long-unburnt sites, i.e. more dissimilar than null

expectations (Fig. 6a, b, e), while the beetles in the recently-burnt sites (Fig. 6c) and

wasps in the twice-burnt sites (Fig. 6f). Finally, the fly b-deviations were close to zero in

recently-burnt sites (once and twice) and significantly lower in long-unburnt sites

(Fig. 6d).

Fig. 4 Mean effect plots of abundance-based within fire-history regime dissimilarity estimated by Bray–Curtis index (mean ± standard error) as a function of fire-history regime showing the results of formulatedGeneralized linear models predicting within fire-history regime dissimilarity as a function of distancebetween sites and fire history for (a) flower-visitor community, and for each guild (b–f). Different lettersindicate significant differences between fire-history regimes, according to GLM analysis. Fire-historyregime abbreviations: TB = twice-burnt sites, RB = recently-burnt sites, LUB = long-unburnt sites (old-burntand unburnt sites)

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Discussion

Assessment by pantraps of the flower-visitor community in a mixture of post-fire regimes

in Rhodes Island, Greece, revealed significant differences in the abundance of fly and

sawfly guilds and the entire flower-visitor community, which exhibited their highest

abundances in recently-burnt sites. However, we found no significant differences in bee,

beetle, and wasp abundance, as well as in species richness of any flower-visitor guild. This

is not consistent with the reported patterns of diversity peaks in the early post-fire years

(Petanidou and Ellis 1996; Potts et al. 2003; Cruz-Sanchez et al. 2011). The lack of

significant differences is likely due to the fact that we sampled 4 years after the most recent

fire, therefore potential early post-fire years’ patterns remained undetected. Interestingly,

however, several studies found no effect of fire on insect diversity, such as in arthropods in

Swiss temperate forests at different time intervals following single fires ranging from 1 to

24 years (Moretti et al. 2006), spheciform wasps in a Mediterranean agroecosystem with

time elapsed since last fire ranging from 1 to 13 years (Cruz-Sanchez et al. 2014), insects

in Mediterranean forests at early post-fire years (Elia et al. 2012), as well as bees and wasps

in unburnt and recently burnt (3–5 years ago) managed boreal forests (Rubene et al. 2015).

Fire strongly affected species community structure of each flower-visitor guild in terms

of abundance except for flies and wasps, thus resulting in changes in species composition

as has been repeatedly documented (Potts et al. 2003; Moretti et al. 2006; Cruz-Sanchez

et al. 2014; Bogusch et al. 2015; Rubene et al. 2015). The spatial arrangement of sites also

had significant effects on species community structure, but pairwise comparisons did not

Fig. 5 Mean effect plots of presence/absence-based Jaccard b-deviation (mean ± standard error) as afunction of fire-history regime showing the results of formulated Generalized Linear Models predictingwithin fire-history regime b-deviation as a function of distance between sites and fire history for (a) flower-visitor community, and of each guild (b–f). Different letters indicate significant differences between fire-history regimes, according to GLM analysis. Fire-history regime abbreviations: TB = twice-burnt sites,RB = recently-burnt sites, LUB = long-unburnt sites (old-burnt and unburnt sites)

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reveal a general pattern. Although many species occurred almost exclusively in only one

fire-history regime (commonly represented by only one or two individuals), multivariate

GLM analysis showed that the abundance of these rare species did not contribute to fire-

driven changes of community structure. The seven beetle and the one sawfly species

responding significantly to fire according to univariate tests of multivariate GLM belonged

to the most abundant and common ones, with most of them more abundant in recently-

burnt sites. Although fire history had a significant effect on bee community structure, the

abundance of bees, the most prominent pollinators, did not vary significantly among dif-

ferent fire-history regimes regarding the abundance of their common species. Considering

that pollination success is positively related to pollinator abundance (Vazquez et al. 2005)

and rare species may be functionally unimportant (Winfree et al. 2015), the above imply

that provision of pollination services may not be considerably affected by fire in our case

study.

The species composition in burnt sites was more similar (lower b-diversity) compared

to long-unburnt sites. This is in accordance with previous studies which showed that

disturbances lead to convergence in community composition (Tylianakis et al. 2006;

Quintero et al. 2010). The pattern was observed in all flower-visitor insects examined,

except flies. This pattern was more apparent when considering the abundance-based metric

of b-diversity and less prominent in the presence/absence-based metric. Furthermore, the

presence/absence b-deviations showed that species composition is comparable to the

expectations under random assembly processes. This finding indicates that observed dif-

ferences are due to the large number of unique species in fire-history regimes, represented

Fig. 6 Mean effect plots of abundance-based Bray-Curtis b-deviation (mean ± standard error) as afunction of fire-history regime showing the results of formulated Generalized linear models predictingwithin-fire history regime b-deviation as a function of distance between sites and fire history for (a) flower-visitor community, and of each guild (b–f). Different letters indicate significant differences between fire-history regimes, according to GLM analysis. Fire-history regime abbreviations: TB = twice-burnt sites, RB= recently-burnt sites, LUB = long-unburnt sites (old-burnt and unburnt sites)

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primarily by one or few individuals, given that the communities across different fire-

history regimes are subsets of the same species pool. However, the abundance-based b-deviation was higher than null expectations, implying that fire-history regimes differ in the

spatial distribution of individuals. This, in turn, may reflect differences in resource

availability across fire regimes, since species diversity is linked to habitat diversity, while

species abundance is linked to the quantity of the resource.

Interestingly, there was greater convergence of species composition (lower within fire-

history regime dissimilarity) in recently-burnt sites compared to twice-burnt ones, high-

lighting the role of fire frequency in shaping diversity patterns of flower-visiting insects.

This may reflect the differential availability and spatial arrangement of fuels before the

2008 fire at those regimes, considering that fuel accumulation is a major determinant of fire

intensity and impact. Having had experienced a major fire event 16–24 years before the

2008 fire, the twice-burnt sites were exposed to a lower severity fire versus the recently-

burnt sites due to the limiting time interval for fuel accumulation. Furthermore, patches in

the twice-burnt sites may have acted as fire refuges leading to a more heterogeneous post-

fire mosaic and thus a species composition of higher heterogeneity.

Contrary to the situation in the twice-burnt sites, the absence of fire in the recently-burnt

sites in the last 50 years before the 2008 fire event lead to an increased fuel amount and

canopy closure. More fuel accumulation may have facilitated an intense and evenly dis-

tributed fire, resulting in more homogenous post-fire ambient and thus to a greater

homogenization of species composition. These findings suggest that forest managers

should take into consideration the time elapsed since the last fire event, the frequency of

fire events and arrange for reduction of fuel accumulation by various methods to ensure

more diverse assemblages of flower-visiting insects. This is especially important under the

scenario of climate change, which is expected to dramatically affect fire patterns and

frequencies especially in the Mediterranean (Pausas and Paula 2012).

Bees showed similar levels of dissimilarity in recently-burnt and twice-burnt sites,

which may reflect the highly dissimilar foraging ranges of different bee guilds, including

bumblebees with wide foraging range (Gathmann and Tscharntke 2002; Westphal et al.

2006) versus beetles (Englund 1993) and the remaining taxa examined. This certainly

results from the fact that between insect guilds showing the same degree of aggregation,

those with larger foraging ranges exhibit more similar species composition compared to

guilds with shorter foraging ranges, because the former may forage and be recorded in

locations far from their nesting sites. This would explain why the pattern is not observed in

flower-visitor guilds with higher average dispersal abilities and wider foraging ranges such

as bees.

Our results highlight the importance of the time elapsed since the last fire event for

variation in species composition as the long-unburnt sites consistently displayed higher b-diversity compared to burnt sites. Perhaps, b-diversity differences are driven by regional

species richness (at fire-history regime level), given that regimes did not differ significantly

in mean a-diversity (species richness at site level). The null modelling approach revealed

that neutral effects and not environmental filtering drive this pattern in terms of species

presences. This finding may imply that generalists are favored, while specialists are dis-

advantaged and therefore are in greater need of conservation. This is an important con-

servation concern under the scenario of climate change where specialists are likely to face

greater risk (Warren et al. 2001).

In summary, our analysis showed that fire-history strongly affected species community

composition of most flower-visitor guilds (except flies and wasps), but had no significant

effect in mean values of abundance and richness in most cases. Fire led to convergence of

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species composition with frequency and time elapsed since the last fire event in shaping

diversity patterns of flower-visiting insects. The observed high neutral presence/absence b-diversity implies that in order to preserve as many species as possible, conservation should

give priority to sites of high diversity (Socolar et al. 2016).

Acknowledgments This research has been co-financed by the European Union (European Social Fund–ESF) and Greek national funds through the Operational Program ‘‘Education and Lifelong Learning’’ of theNational Strategic Reference Framework (NSRF)—Research Funding Program: THALES-Investing inknowledge society through the European Social Fund (Grant Number: 376737). We thank H. Dathe, J. Dils,A. Ebmer, D. Michez, A. Muller, A. Pauly, C. Praz, M. Quaranta, S. Risch, W. Schedl, E. Scheuchl, M.Schwarz, and A. Vujic for insect identification.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

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