Climatic Correlates of Body Size in European Tenebrionid Beetles (Coleoptera: Tenebrionidae)

Org Divers Evol (2014) 14:215–224 DOI 10.1007/s13127-013-0164-0

ORIGINAL ARTICLE

Climatic correlates of body size in European tenebrionid beetles (Coleoptera: Tenebrionidae)

Simone Fattorini & Roberto Lo Monaco & Andrea Di Giulio & Werner Ulrich

Received: 17 June 2013 /Accepted: 4 December 2013 /Published online: 29 December 2013 # Gesellschaft für Biologische Systematik 2014

Abstract Tenebrionidae are one of the largest families of the second hypothesis, we regressed mean body size of beetles and are known for their adaptations to hot and dry European country faunas against climatic characteristics. We climates. An increase in body size also increases the volume/ found a strong increase in body size in southern faunas surface area ratio, which reduces transpiration, and hence experiencing hot and dry climates. Therefore, increase in body water loss. If an increase in body size is an important adapta- size is not a major adaptation in tenebrionid evolution, but tion in tenebrionids to cope with increasing aridity, we expect climate is an important filtering factor that determines a prev- a correlation between body size and climatic gradients in the alence of larger species in southern Europe. major tenebrionid clades. Alternatively, we can postulate that arid climates do not drive body size evolution, but rather Keywords Biogeography . Body size . Europe . Darkling select, from a wider fauna containing species of any size, beetles . Macroecology those that have larger bodies. In this case we expect that drier regions will host faunas that contain, on average, larger species. To test the first hypothesis, we correlated inter-specific Introduction body size variation in the main tenebrionid clades with climatic gradients in Europe. We found only weak trends. To test The family Tenebrionidae is one of the largest of Coleoptera, comprising about 19,000 known species (Aalbu et al. 2002). Adult tenebrionids exhibit a diversity of form possibly ex- Electronic supplementary material The online version of this article (doi:10.1007/s13127-013-0164-0) contains supplementary material, ceeding that of any other family of beetles. Tenebrionidae which is available to authorized users. occur in all major zoogeographical regions and are strongly represented also in hot deserts, where other insects are scarce. S. Fattorini Azorean Biodiversity Group (CITA-A) and Platform for Enhancing In general, tenebrionid species inhabiting environments char- Ecological Research & Sustainability (PEERS), University of the acterized by high temperatures and low precipitations exhibit Azores, Angra do Heroísmo, Terceira, Açores, Portugal a number of well-known morphological, physiological and behavioral adaptations to cope with the risk of overheating S. Fattorini (*) Department of Biotechnology and Biosciences, University of Milano and dehydration, like subelytral cavity, sand-walking and Bicocca, Piazza della Scienza 2, 20126 Milan, Italy sand-swimming modifications, wax bloom covering the in- e-mail: [email protected] tegument to minimize water loss, drinking of fog water, active uptake of atmospheric water, use of metabolic water, high R. Lo Monaco : A. Di Giulio Department of Sciences, University of Roma Tre, Viale G. Marconi specialized osmoregulation processes, etc. (see Fattorini 446, 00146 Rome, Italy 2000, 2008 for reviews). A. Di Giulio An increased body size in insects living in arid environ- e-mail: [email protected] ments, in either cold or warm regions, has also been interpreted repeatedly as an adaptation to reduce water loss, W. Ulrich because an increase in the volume/surface area ratio reduces Ecology and Biogeography, Nicolaus Copernicus University in Toruń, Lwowska 1, 87-100 Toruń, Poland transpiration (Chown 1993;Hadley1994). In fact, it has been e-mail: [email protected] suggested, on anecdotal evidence, that tenebrionids living in 216 S. Fattorini et al. warm and arid environments tend to be particularly large promoting the prevalence of large species in arid areas. (Marcuzzi 1960), but this issue has been largely unexplored. If this is correct, we expect the average body size of the At the intraspecific level, Doyen and Rogers (1984)found species that constitute a fauna to increase with increasing some clinal variation in body size in a tenebrionid species temperatures and decreasing precipitation in the area living in western North American sand dunes, but the factors where that fauna lives. involved in these spatial variations remained undetected. Krasnov et al. (1996) found variation in body size with eleva- To explicitly test these two hypotheses, we used variation tion in certain (but not all) tenebrionid species inhabiting the in the body size of European tenebrionids. Tenebrionids are Negev Desert—the largest individuals occurring at low and widespread across Europe and their distribution is strongly warmer sites. They interpreted this trend as a possible adap- conditioned by climatic factors (Fattorini and Baselga 2012; tation for thermoregulation, because larger individuals have Fattorini and Ulrich 2012a, b). To test the aforementioned small surface/volume ratio and absorb relatively less direct hypotheses about the effects of temperature and precipitation shortwave and visible radiation, being thus in a better situation gradients on tenebrionid body size, we used two complemen- than smaller individuals at high ambient temperatures. Finally, tary approaches. To test the first (adaptive) hypothesis, we in a study that mixed intra- and inter-specific variation, De Los regressed the body size of each species against the mean Santos et al. (2000) found that, in the genus Hegeter of values of temperatures recorded from the areas inhabited by Tenerife Island, individuals from the lower zones adopted that species. We conducted separate analyses for taxonomi- globular and robust forms, possibly to avoid moisture and cally homogeneous groups to disentangle true adaptation from temperature stress. lineage turnover (Olson et al. 2009; Homburg et al. 2012). To All these studies on Tenebrionidae have been conducted at test the second (filtering) hypothesis, we calculated values of local scale and were focused on population variations, where- the mean body size of local faunas (sensu Penev 1996), i.e., as no research has been performed to test variation in body the mean of the body size of the species that live in each area, size among species at broad spatial scale. Studies on other and correlated these mean values with temperature values of arthropod taxa (e.g., Peat et al. 2005; Entling et al. 2010; each area (see Knouft 2004 for a similar approach). Ulrich and Fiera 2010) suggested that large body size is With this second approach, we tested if colder regions host favored by high temperature and low precipitation. species are, on average, larger than those inhabiting warmer Therefore we can expect large-scale spatial variation in tene- areas. The idea is that temperatures select species according to brionid body size across Europe. In fact, two main hypothesis body size from a common pool. Thus, we assume the whole can be evoked to explain the observation that the largest European fauna as a common pool of species from which tenebrionids tend to occur in hot and dry areas: northern countries were colonized after the last Pleistocene glaciations (Fattorini and Ulrich 2012b). If higher tempera- (1) Trend of increasing body size with temperature is a tures and low precipitation favor species with larger body size, consequence of an adaptive increase in size to cope with we expect a positive correlation between the mean body size increasing aridity. of the species that compose a fauna of a given area and the According to this interpretation, within each clade, climatic conditions of that area. species living in warmer and dryer areas should be larger than their counterparts living in colder and more humid places. Thus, on a large geographical scale, we expect, Materials and methods within each clade, an inter-specific cline of increasing body size with increasing temperatures and decreasing The current taxonomic division into species and subspecies, as precipitation among species of a given clade. applied to the tenebrionids of Europe, is arguably arbitrary. (2) Faunas inhabiting warmer and drier areas contain, on Recent morphological (Trichas 2008; Condamine et al. 2011; average, larger species because of filtering processes that Ferrer 2008, 2011) and molecular (Pons et al. 2004;Soldati favor, from the various clades that occur in each region, and Soldati 2006;Stroscioetal.2011) analyses showed that species having larger body size. populations traditionally classified as subspecies are really In this case, we expect that there is no clear trend in ‘evolutionarily significant units’ (sensu Ryder 1986), usually body size variation within each particular clade, and that demanding a species status. Thus, we considered both species faunas include species that may have any size, although and subspecies as terminal taxonomic units. Species and sub- certain faunas should be characterized by the prevalence species will be referred to as ‘species’ for simplicity. Further, of large-sized species. If large-sized species are favored the present paper includes the former family Lagriidae as a in warmer and drier areas, they will be a prevalent subfamily within the Tenebrionidae. In consideration of the component of the local fauna in such areas but not in highly derivative and specialized characters of Alleculinae others. Thus, climate acts as a filter on body size, (formerly considered a separate family of winged and flower- Climatic correlates of body size in European tenebrionid beetles (Coleoptera: Tenebrionidae) 217

visiting beetles), we did not consider them in our database. precipitation. We used NT<0 as a measure of duration of cold Moreover, distributional data for alleculines are definitively less climatic conditions during the year. In general, we predict that reliable than those obtained for the other Tenebrionidae. the longer the time for which temperatures are very low, the There are various tenebrionid species that are synanthropic, smaller the insect body size, again in response to oxygen being associated with human food, and which have become dissipation constraints. ΔT can be considered a measure of cosmopolitan (e.g., various species belonging to the genera climatic variability. Here we do not formulate any physiological Tenebrio, Tribolium, Alphitobius, Alphitophagus, prediction, but we can imagine that, because tenebrionids find Latheticus, etc.). So it can be assumed that their distribution shelter under bark or under stones during adverse climatic (very in Europe is strongly dependent on human activities. cold or very hot) conditions, small body sizes should be favored Therefore, we excluded these species from our analyses. in areas with higher ΔT values, because smaller species should Likewise, we did not consider citations of certain species find shelter more easily than large sized species. To test the due to recent and documented introductions. Finally, we al- adaptive hypothesis, we calculated, for each species, the mean ways excluded doubtful data because of taxonomic problems, value of these climatic variablesacrossallcountriesfromwhich misidentifications, or ancient unconfirmed records. the species was recorded. Then, we regressed species body size We considered the faunal composition of native tenebrionid against climatic variables and used the corrected Akaike infor- species from 34 European mainland areas as given in Fattorini mation criterion (AICc) for model choice. and Ulrich (2012a, b) for a total of 1,390 species. In general, Although species dependence on temperature is frequently these areas correspond to European countries, but some coun- expressed by the average temperature of the species’ range tries were split or aggregated on the basis of biogeographical (see, for example, the species temperature index used by criteria and data availability (see Baselga 2008; Fattorini and Devictor et al. 2012), use of average values might obscure Ulrich 2012a, b). For simplicity, all these territorial units are the importance of “extreme” conditions. For example, a spe- hereafter referred to as “countries.” This matrix of species cies that can survive with the same success from the extreme presence/absence per country was revised to take into account north to the extreme south of Europe, would score mid- new data and taxonomic changes (see Online Resource 1). For average climatic variables similar to those experienced by a each species we compiled data on the mean body length of species with a reduced, central European distribution. In some European tenebrionids from literature sources, including cata- cases, the mean temperature experienced by a species living logues, taxonomic revisions, identification keys, and original all over Europe could be higher than that of a species occu- descriptions, for a total of 360 scrutinized references. pying only a northern country and equal to a species occupy- For each of the 34 considered mainland areas, we used the ing only a central country. Thus, in addition to the aforemen- following climate variables (Fattorini and Ulrich 2012a, b): tioned mean values, we calculated minimum and maximum average annual temperature (T mean), average temperature in climatic factors “experienced” by each species across its July (TJuly), average temperature in January (TJanuary), yearly European range. For this, we considered: (1) the maximum temperature difference (ΔT=T July – T January) and average temperature value found among the monthly mean tempera- number of days with temperatures below zero (NT<0)asan ture values of July recorded in the 34 investigated areas estimate of winter length (see Online Resource 2). In addition (MaxTJuly); (2) the minimum temperature value found among to these temperature variables we also included annual pre- the monthly mean temperature values of January cipitation (P). These variables have been selected to express (minTJanuary); (3) the differences between these two extreme different possible effects of temperatures on body size. In values (ΔTMax); (4) the maximum number of days with tem- general, we expect a positive relationship between body size perature below 0°C found among the values recorded in the 34 and Tmean, and a negative relationship with P. T January indi- investigated areas (MaxNT<0); (5) the minimum number of cates how cold a region is in winter. Thus, we expect a positive days with temperature below 0°C found among the values relationship between body size and TJanuary because of the recorded in the 34 investigated areas (minNT<0); (6) the dif- (semi-)passive oxygen dissipation constraints, that implies a ference between these two extreme values (ΔN T<0Max); (7) the more effective cell functioning at higher temperatures maximum value of precipitation found in the 34 investigated (Speight et al. 2008). If large-sized bodies evolve as a re- areas (MaxP); (8) the minimum value of precipitation (minP); sponse to very high temperatures and low precipitation, we and (9) the difference between these two extreme values (ΔP). also expect an increase in body size with increasing TJuly, We have excluded species present in only one area which are usually the highest temperatures during the year, (endemics), because these species have only one value for and a decrease with increasing precipitation. We expect that each of the aforementioned variables, so there is no geograph- these patterns should be more pronounced in clades composed ical variability in the experienced climatic conditions at our mainly of ground-dwelling species. For taxonomic groups of scale of analysis. mainly arboreal species, which are therefore adapted to more We run separate analyses for all species, endemics, tribes, humid climate, we predict that body size might increase with and the subfamily Pimeliinae. We considered the tribal level 218 S. Fattorini et al.

(according to Löbl and Smetana 2008) to test the adaptive Results hypothesis due to the close phylogenetic relatedness. Current information indicates that the tribes used in tenebrionid Adaptive hypothesis taxonomy are substantially monophyletic units. For example, the tenebrionid clades found by Doyen and Correlations between average climate factors and body length Tschinkel (1982) and Doyen (1993) in their phylogenet- explained less than 5% of variance in all but one case ic reconstruction largely fit traditional tribes. Also, mor- (Table 1) and thus did not corroborate strong adaptive phological analyses of the mouthparts of Pimeliinae processes. Nevertheless, we found some, albeit weak, based on comparison of several genera within major recurrent trends. The number of days below zero, the tribes revealed that there is minimal variation among absolute annual temperature difference, and annual pre- genera belonging to the same tribe, whereas between-tribe cipitation were negatively correlated with body length. differences are very strong (S. F, and A. Di G., unpublished January, July, and annual average temperature correlated data). Thus, tribes appear a particularly suitable systematic positively (Table 1). These results indicate a certain level to use as proxy of true clades for our analyses (see also tendency of body size to decrease with increasing num- Fattorini et al. 2013a). ber of cold days (especially in Helopini), climatic var- For species assignment to tribes we followed Löbl and iability and precipitation, whereas body size tends to Smetana (2008). We considered only tribes that had, in our increase with temperature. database, at least 30 species (an arbitrary cut-off value to be A model selection procedure based on AICc values, iden- confidently protected by the central limit theorem). We tested tified for the complete (all species) dataset a model including the Pimeliinae separately because they exhibit the most strik- NT<0, Tmean and P as a best fit model (Table 2). If P is not ing adaptation to arid environments, where they are very included among the possible predictors, a best model included abundant and diversified (Doyen and Tschinkel 1982; N T<0, ΔT, T July,andT mean. However, this model is not Doyen 1993; Fattorini 2000). Thus, we conducted a compar- substantially better than other models than included a different ative analysis for the whole pimeliine clade against the re- selection of climatic variables (but which always included maining tenebrionids, which include lineages that may have N T<0 and T mean; results not shown). When only endemic very different climatic preferences. Also, non-Pimeliinae are, species were considered, a model selection procedure based in our datasets, a substantially monophyletic group, because on AICc values, identified a model including N T<0, ΔT, T Jan, European tenebrionids can be divided into three main clades: and Tmean, as a best fit model (Table 2). Again, this model is one including Pimeliinae, one including Lagriinae, and the not substantially better than other two models with a different last including all other groups. Because the true positon of selection of climatic variables (but which always included

Lagriinae is uncertain (Levkaničová 2009), and they include NT<0 and Tmean; results not shown). For the Pimeliiane, the only 43 species in our dataset , we aggregated them in a non best model included ΔT and P.IfP is not included among the

Pimeliinae group. predictors, the best model included NT<0, TJan, Tmean and TJuly, Statistical significance of regression analysis is influ- and was similar to other two models that included NT<0 e Tmean enced by non-independence of data due to phylogenetic (results not shown). Finally, for the non Pimeliinae, the best autocorrelations (Felsenstein 1985). However, if taxo- model included only TJuly (Table 2). Thus, relationships varied nomically related species are expected to have a more according to the dataset used, but P seems important for similar response to a climatic gradient than unrelated tenebrionids in general and for Pimeliinae in particular, whereas species, developing separate analyses for clades of phy- non Pimeliinae are more influenced by TJuly. logenetically strictly related species (such as tribes in Using “experienced” minimum and maximum values this study) offer the opportunity of disentangling true (Table 3), we found that body size had a positive but small adaptation from lineage turnover (Olson et al. 2009; correlation with minTJanuary, a negative but small correlation Homburg et al. 2012). with ΔTMax, and no correlation with MaxTJuly. We found sig- To test the second (filtering) hypothesis, we calculated, for nificant, but low correlations of body size with both MaxNT<0 each country, the mean value of body length of all the species and ΔN T<0Max, whereas correlation with minNT<0 was very recorded from that country. Then, we regressed these value of close to the probability level. Finally, we found significant, but mean “faunal” body size against the climatic variables. To low, correlations of body size with both MaxP and (ΔP, but not control for spatial autocorrelation we calculated, for each with minP. Using subfamilies and tribes, we found only few geographical unit, the latitude and longitude of its geograph- significant correlations. A model selection procedure based on ical centroid as given in Fattorini and Ulrich (2012b), and used AICc values identified, for non-endemic species, a model in- the simultaneous spatial autoregressive (SAR) model as im- cluding minTJanuary and minNT<0 as a best fit model plemented in SAM 4.0 (Rangel et al. 2010). Again we used (R 2=0.039, AICc=2,912.904). The second model, with an

AICc for model choice. AICc value very close to the first one, included ΔN T<0Max, Climatic correlates of body size in European tenebrionid beetles (Coleoptera: Tenebrionidae) 219

Table 1 Coefficients of correlation between climatic variables and Eu- TJanuary (average January temperature) and TJuly (average July tempera- ropean tenebrionid body length. NT<0 average number of days with ture), Tmean average annual temperature, P annual rainfall temperatures below zero, ΔT yearly temperature difference between

Taxon Number of taxa NT<0 ΔTTJanuary TJuly Tmean P

All species 947 −0.086 ** −0.178 **** 0.116 *** −0.034 0.019 −0.213 **** Endemics 483 −0.013 −0.187 **** −0.002 −0.149 *** −0.128 ** −0.215 **** Pimeliinae 428 −0.094 −0.208 **** 0.059 −0.134 ** −0.088 −0.260**** Asidini 237 −0.118 −0.033 0.118 0.154 * 0.084 −0.214*** Stenosiini 40 −0.061 −0.078 0.105 0.115 0.069 −0.224 Tentyriini 55 −0.032 −0.086 0.085 0.060 0.103 −0.111 Pimeliini 41 −0.059 −0.036 0.132 0.015 0.046 −0.150 Non Pimeliinae 519 −0.050 −0.044 0.071 0.080 0.072 −0.080 Tenebrioninae 391 −0.013 −0.028 0.018 0.003 0.0012 −0.037 Helopini 129 −0.178* −0.024 0.076 0.104 0.119 0.033 Opatrini 39 0.000 −0.102 0.070 0.023 0.032 −0.065 Pedinini 159 −0.043 −0.130 0.115 0.074 0.078 −0.115 Diaperinae 73 −0.107 −0.118 0.145 0.139 0.126 −0.035

Probability levels: * P <0.05; ** P <0.01; *** P <0.001, **** P <0.0001

and MaxP (R2=0.038, AICc=2913.279). In general, analyses Discussion conducted using “experienced” minimum and maximum values produced outcomes similar to those achieved with the average We found that higher temperatures have probably a very weak values, but with lower correlation coefficients and smaller frac- effect on the evolution of larger body size in European tene- tions of explained variance, so they will be not discussed further. brionids. Moreover, patterns vary according to the taxonomic group under consideration. In the tribe Helopini, which in Filtering hypothesis Europe is represented mainly by arboricolous species that find shelter under bark during winter, there is a trend towards a Mean values of body lengths of species assemblages (faunas) reduction in body size with increasing number of days with in Europe decreases with increasing latitude when all species temperatures below 0 °C. This may be a reflection of another are analyzed as a whole, for non Pimeliinae and, albeit less adaptive syndrome determined by the arboreal life style of distinctly, for Pimeliinae (Fig. 1). In accordance with their these tenebrionids: reduction in body size might aid Helopini thermophilic preferences, Pimeliinae are virtually absent from in finding places under bark to overwinter. As ΔT can be areas north to 50°N (in fact, there is only a citation of Asida viewed as an index of climatic seasonality, a negative trend of sabulosa sabulosa (Fuesslin, 1775) at about 50°35′N; Köhler body size suggests that higher climatic variability promotes 1996). A comparison of SAR regressions with OLS regres- reduction in body size. This may reflect various adaptive sions indicates that removal of autocorrelation has a moderate syndromes: smaller species may find resting sites easily or effect on parameter estimates. Moreover, regressions for en- may easily overcome adverse conditions (e.g., lack of food) demics are affected strongly by a single outlier, Sweden, because of their reduced needs. According to the fasting because of the ‘anomalous’ occurrence of an endemic subspe- endurance hypothesis, vertebrates may benefit from growing cies (Blaps sinuaticollis suecica Ferrer & Picka 1990) in this large in unpredictable environments, whereas smaller individ- northern country (see Fattorini and Ulrich 2012a). A model uals should be advantaged in predictable, but food-limited selection procedure including both temperatures and latitude, environments (Meiri et al. 2005). In general, tenebrionids pointed out latitude as an important variable, but in contradict the vertebrate fasting endurance hypothesis, be- association with some temperature variables, for all cause body size tends to decrease with seasonality (expressed groups except Pimeliinae. If latitude is excluded from the by ΔT) and winter severity (expressed by NT<0). For exam- explanatory variables, the obtained best fit models have lower ple, Murphy (1985) found sparrow size to be correlated pos- R2 and larger AICc, but there is a substantial overlap among itively with the annual temperature range, i.e., with more selected climatic variables. Except for endemics, latitude ap- seasonal environments, and explained the correlation by the pears a more important predictor of body size than tempera- less predictable nature of more seasonal habitats, whereas we tures (Table 4). found negative, albeit weak, relationships (Table 1). As 220 S. Fattorini et al.

Table 2 Parameter values, standard errors and associated probability 2 regards annual temperatures, it seems that tenebrionids levels of OLS best fit models for all species (R =0.246, R =0.060, tend to increase their body size with increasing temper- R 2adj=0.057, F=15.155, AICc=5736.353, n =947); endemics (R = 0.303, R2=0.092, R2adj=0.086, F=12.117, AICc=275.769, n =483), ature, but the trend is weak (Table 1). Thus, tempera- Pimeliinae (R =0.274, R 2=0.075, R 2adj=0.073, F=17.238, AICc= tures do not seem to be an important driving force in 2 2 2436.923, n =428), and non Pimeliinae (R =0.080, R =0.006, R adj= body size evolution. 0.006,F=3.348, AICc=3191.991, n =519). Tjan average temperature in Interestingly, tenebrionid body size tends to be correlated January, T average temperature in July, T average annual temper- July mean negatively with precipitations (Table 1) This indicates a cer- ature, ΔT yearly temperature difference between TJanuary and TJuly, NT<0 average number of days with temperatures below zero, P annual rainfall tain tendency towards an increase in body size at decreasing water availability. Weakness of trends, however, suggests that All species body size cannot be considered a strong adaptive syndrome to Coefficient Standard coeffient SE avoid water loss in tenebrionid beetles, although it may con- Constant 16.901 0.000 1.355 tribute to reduce dehydration in conjunction with other, and NT<0 0.012 0.067 0.009 probably much more important, adaptations to obtain and TJan 0.493 0.347 0.134 maintain water, such as morphological (e.g., color, integument − − Tmean 0.459 0.247 0.139 structure, wax blooms, subelytral chambers, spiracle morphol- − − P 0.050 0.143 0.013 ogy, leg length, etc.), physiological (e.g., use of metabolic Endemics water obtained from fats), and behavioral (nocturnal activity, Coefficient Standard coeffient SE estivation) adaptations (see Fattorini 2008). Interestingly, Constant 17.195 0.000 1.296 Helopini, which include many arboreal species, were NT<0 0.022 0.130 0.012 the only group that showed an increase in body size with ΔT 0.604 0.413 0.225 increasing precipitation. TJan 2.107 1.256 0.424 In a study on the intra-specific variation in elytral and − − Tmean 2.114 1.316 0.443 femur lengths of seven tenebrionid species along an elevation Pimeliinae gradient in the Ramon erosion cirque (Israel), Krasnov et al. Coefficient Standard coeffient SE (1996) found a support for increasing body size with increas- Constant 18.225 0.000 1.019 ing temperature in six analyses; a converse pattern for the for ΔT −0.125 −0.100 0.068 elytral length of one species; and no relationship between P −0.060 −0.208 0.016 length and elevation in the remaining nine analyses . Thus, Non Pimeliinae even at intra-specific level, body size is not an important Coefficient Standard coeffient SE adaptive syndrome in tenebrionids. Constant 5.385 0.000 2.363 Our faunal approach clearly demonstrates that tenebrionid

TJuly 0.187 0.080 0.102 faunas at lower latitudes tend to be composed of species that are, on average, larger than those that inhabit northern

Table 3 Coefficients of correlation between “extreme” climatic variables recorded among the study areas, minTJanuary minimum value recorded and European tenebrionid body length. MaxNT<0 maximum value re- for the average January temperatures (TJanuary), ΔTMax difference between corded for the average number of days with temperatures below zero MaxTJuly and minTJanuary, MaxP maximum value recorded among the (NT<0) among the study areas, minNT<0 minimum value recorded for annual rainfall values (P), minP minimum value recorded among the NT<0, ΔN T<0Max difference between MaxNT<0 and minNT<0, MaxTJuly annual rainfall values (P), ΔP difference between MaxP and minP maximum value recorded for the average July temperatures (T July)

Taxon No. of taxa MaxNT<0 minNT<0 ΔNT<0Max MaxTJuly minTJanuary ΔTMax MaxP MinP ΔP

All non-endemic species 464 −0.128** 0.093* −0.175**** −0.051 0.167*** −0.178**** −0.174**** 0.0131 −0.175**** Pimeliinae 133 −0.055 0.110 −0.155**** −0.049 0.155 −0.180* −0.227* −0.526 −0.205* Tentyriini 30 0.207 0.090 0.131 −0.026 −0.069 0.060 0.046 0.050 0.012 Non Pimeliinae 331 −0.103 0.039 −0.116* −0.023 0.101 −0.104 −0.091 0.013 −0.093 Tenebrioninae 234 −0.012 0.025 −0.028 −0.024 0.006 −0.016 −0.004 0.039 −0.025 Helopini 76 −0.070 −0.176 0.071 0.082 0.118 −0.069 −0.035 0.045 −0.070 Opatrini 32 −0.084 −0.111 −0.010 0.080 0.071 −0.034 0.133 0.069 0.099 Pedinini 73 −0.121 0.046 −0.162 −0.082 0.227 −0.280* −0.157 0.015 −0.167 Diaperinae 53 −0.219 0.019 −0.186 0.030 0.221 −0.184 −0.110 −0.033 −0.068

Probability levels: * P <0.05; ** P <0.01; *** P <0.001, **** P <0.0001 Climatic correlates of body size in European tenebrionid beetles (Coleoptera: Tenebrionidae) 221

Fig. 1 a–d Relationships between latitude and mean body length of tenebrionid faunas in European countries. Both OLS and SAR regression lines are shown. Equation parameters are reported here only for OLS regressions. SAR parameters are given in Table 3 a All species (y =−0.1865x+17.695, R2=0.7256). b Endemics (y =0.4527x −9.7867, R2=0.3526). c Pimeliinae (y =−0.107x+16.157, R2=0.0238). d Non Pimeliinae (y =−0.1489x+15.59, R2=0.7246). Dotted lines OLS regressions. Solid lines SAR regressions

countries. Latitude itself, however, does not influence any rule, as postulated for the presence of larger Scarabaeinae in biological characteristics, and correlation between latitude the Paleotropical region (Davis et al. 2002)andlarger and size reflects selective forces that covary with latitude Aphodiini in the Palearctic region (Cabrero-Sañudo 2012), (Meiri et al. 2005). Temperatures are the most obvious vari- although this hypothesis is at present very speculative because ables that show a latitudinal gradient. Although we found that of the lack of adequate phylogenetic reconstructions. correlation between latitude and faunal mean body size is On the other hand, temperatures exert a strong influence in largely an effect of temperature gradients, our results also determining faunas with a larger fraction of large-sized species suggest that the selected climatic variables tend to have a in warmer areas. Thus, temperature gradients in Europe act as a lower explanatory power when compared with latitude alone. “filtering” factor: although body size of individual species is This may imply either (1) that there are climatic effects sub- barely affected by temperatures; higher temperatures increase sumed by latitude but not expressed by our temperature mea- the contribution of large-sized species in a fauna. This type of sures or (2) that there is some non-thermal gradient or bias relationship may be a reflection of the fact that areas associated with latitude. A possible indication comes from with higher temperatures may be colonized more easily Pimeliinae. This subfamily includes the tribe Pimeliini, which by large-sized species, which are more resistant to des- are among the largest tenebrionids. As Pimeliini have a mainly iccation, whereas these species are less favoured in African distribution, with relatively few species reaching northern countries. southern Europe, this can create a taxonomic bias. In addition to the better ability of large-sized species to Moreover, the occurrence of larger species in southern areas cope with desiccation, the preponderance of large-sized spe- can be could be a consequence of the presence of ancient cies in the warmest areas may be a reflection of a thermal lineages (Cope’s rule: taxa increase in body size over evolu- constraint, i.e., the warming-up time. It is well known that, in tionary time; Cope 1887; see Lomolino et al. 2010 for a general, insects cannot perform certain activities until their review). In general, European tenebrionids dispersed north- body has reached a certain temperature, and larger insects heat wards from southern Pleistocene refugia (Fattorini and Ulrich less rapidly than smaller ones (Digby 1955;Stevenson1985). 2012b) and, at least for Pimeliinae, southern European faunas Thus, a large insect can have difficult warming up if weather derived from African clades (see Fattorini 2000). Thus, spe- conditions become suitable only for short time periods, as cies belonging to clades concentrated in southern Europe, often occurs during spring–summer in Northern Europe. So, such as Pimeliini, may be larger as a consequence of Cope’s smaller species can be more opportunistic and successful in 222

Table 4 Parameters values, standard errors and associated probability levels of autoregressive (SAR) models including: Latitude only as explanatory variables for all species (R2 =0.813; AICc=76.983; n = 34), endemics (R2 =0.410; AICc=86.644; n =14), Pimeliinae (R2 =0.197; AICc=106.239; n =21) and non Pimeliinae (R2 =0.707; AICc=77.020; n =3 4) species; both latitude and climatic variables for all species (R2 =0.584; AICc=69.240; n =34), endemics (R2 =0.719; AICc=81.324; n =14), Pimeliinae (R2 =0.153; AICc=105.604; n =21) and non Pimeliinae (R2 =0.789; AICc=71.600; n =34) species; and climatic only variables for all species (R2 =0.536; AICc=110.623; n =34), endemics (R2 =0.346; AICc=93.129; n =14), Pimeliinae (R2 =0.153; AICc =105.604; n =21) and non Pimeliinae (R2 =0.527; AICc=96.029; n =34) species. T jan average temperature in January, TJuly average temperature in July, Tmean average annual temperature, ΔT yearly temperature difference between TJanuary and TJuly, NT<0 average number of days with temperatures below zero

Latitude only Latitude and climate Climate only

Allspecies Allspecies Allspecies Variable SAR coefficient Standard error Variable SAR coefficient Standard error Variable SAR coefficient Standard error Constant 18.916 1.457 Constant 18.344 1.766 Constant 3.380 1.836

Latitude −0.186 0.026 Latitude −0.217 0.031 Tmean 0.402 0.099 Tjan 0.120 0.064 NT<0 0.014 0.008 NT<0 0.019 0.007 Endemics Endemics Endemics Variable SAR coefficient Standard error Variable SAR coefficient Standard error Variable SAR coefficient Standard error Constant 1.528 10.326 Constant −22.390 11.064 Constant 25.133 9.917

Latitude 0.337 0.179 Latitude 0.751 0.192 TJan 0.437 0.783 TJan 0.701 0.668 Tmean −0.617 1.100 Pimeliinae Pimeliinae Pimeliinae Variable SR coefficient Standard error Variable SAR coefficient Standard error Variable SAR coefficient Standard error Constant 20.131 8.210 Constant 15.352 3.379 Constant 15.352 3.379 Latitude −0.183 0.177 ΔT −0.187 0.177 ΔT −0.187 0.177 Non Pimeliinae Non Pimeliinae Non Pimeliinae Variable SAR coefficient Standard error Variable SAR coefficient Standard error Variable SAR coefficient Standard error Constant 15.171 1.187 Constant 13.388 2.459 Constant 3.688 1.330

Latitude −0.139 0.021 Latitude −0.154 0.029 TJan −0.204 0.096 TJul 0.084 0.063 Tmean 0.434 0.130 NT<0 0.010 0.004 .Ftoiie al. et Fattorini S. Climatic correlates of body size in European tenebrionid beetles (Coleoptera: Tenebrionidae) 223 northern areas, since they have smaller bodies to heat and can geographic and taxonomic data. In L. Stevens (Ed.), Global ad- – take advantage of short warming periods. Conversely, in vances in biogeography (pp. 329 360). Rijeka: InTech. Chown, S. L. (1993). Desiccation resistance in six sub-Antarctic weevils southern regions, milder climate conditions probably make (Coleoptera: Curculionidae): humidity as an abiotic factor influenc- such an advantage useless, since most species can find suit- ing assemblage structure. Functional Ecology, 7,318–325. able temperatures through most of their active season. Condamine, F. L., Soldati, L., Rasplus, J.-Y., & Kergoat, G. J. (2011). Moreover, a large size can cope better with overheating when New insights on systematics and phylogenetics of Mediterranean Blaps species (Coleoptera: Tenebrionidae: Blaptini), assessed individuals are exposed momentarily to high temperatures through morphology and dense taxon sampling. Systematic (e.g., when they move on the ground during day-time in open, Entomology, 36,340–361. highly sunny areas, as typical of Mediterranean ecosystems). Cope, E. D. (1887). The origin of the fittest: essays on evolution.New Our filtering hypothesis is also consistent with the nested York: Appleton. Davis, A. L. V., Scholtz, C. H., & Philips, T. K. (2002). Historical pattern of tenebrionid species distribution in Europe. If the biogeography of scarabaeine dung beetles. Journal of tenebrionid of Europe did not show a nested pattern of distri- Biogeography, 29,1217–1256. bution, with northern faunas including a large number of De Los Santos, A., Gómez-González, L. A., Alonso, C., Arbelo, C. D., & species that did not occur in the south, the adaptive concept De Nicolás, J. P. (2000). Adaptive trends of darkling beetles (Col. Tenebrionidae) on environmental gradients on the island of Tenerife would apply. In this case, these northern endemics would have (Canary Islands). Journal of Arid Environments, 45,85–98. been evolved there, or somewhere else, in colder conditions Devictor, V., van Swaay, C., Brereton, T., Brotons, L., Chamberlain, D., and then “selected” their optimal size. But, this is not the case Heliölä, J., et al. (2012). Differences in the climatic debts of birds of the European tenebrionids. There are virtually no tenebri- and butterflies at a continental scale. Nature Climate Change, 2, 121–124. onids endemic to northern countries, and most species cur- Digby, P. S. B. (1955). Factors affecting the temperature excess of insects rently occurring in northern and central Europe are nested in sunshine. Journal of Experimental Biology, 32,279–298. subsets of faunas occurring in southern areas that acted as Doyen, J. T. (1993). Cladistic relationships among Pimeliine glacial refugia (Fattorini and Ulrich 2012a,b). After deglacia- Tenebrionidae (Coleoptera). Journal of the New York Entomological Society, 101,443–514. tion, northern and central areas were colonized selectively by Doyen, J. T., & Rogers, E. (1984). Environmental determinants of size more tolerant and possibly smaller species coming from variation in Eusattus muricatus (Coleoptera: Tenebrionidae). southern refugia (see Fattorini et al. 2013b). This suggests JournaloftheKansasEntomologicalSociety,57(3), 483–489. that smaller species were selectively more able than larger Doyen, J. T., & Tschinkel, W. R. (1982). Phenetic and cladistic relationships among tenebrionid beetles (Coleoptera). Systematic ones to colonize northern Europe, but they did not evolve any Entomology, 7,127–183. adaptive trait, as postulated by our filtering hypothesis. Entling, W., Schmidt-Entling, M. H., Bacher, S., Brandl, R., & Nentwig, W. (2010). Body size - climate relationships of European spiders. Journal of Biogeography, 37,477–485. Acknowledgments WeareparticularlygratefultoM.Lilligforhis Fattorini, S. (2000). Dispersal, vicariance and refuges in the Anatolian invaluable help in finding many references reporting body length mea- Pimeliinae (Coleoptera, Tenebrionidae): remarks on some biogeo- sures. We thank the following people for providing unpublished faunal graphical tenets. Biogeographia, 21,355–398. data and/or for checking regional faunal lists used in this study: O. R. Fattorini, S. (2008). Ecology and conservation of tenebrionid beetles in Alexandrovitch (Belarus), B. Gustafsson (Denmark, Norway, Finland, Mediterranean coastal areas. In S. Fattorini (Ed.), Insect ecology and Sweden), P. Leo (France, Italy, Greece, Spain, overall distribution of conservation (pp. 165–297). Trivandrum: Research Signpost. many species and comments about completeness of inventories), and F. Fattorini, S., & Baselga, A. (2012). Species richness and turnover patterns Soldati (France, Italy, Romania, Greece), who also provided some body in European tenebrionid beetles. Insect Conservation and Diversity, length measures. We are very grateful to two anonymous referees for their 5,331–345. constructive comments. H. Pearson kindly improved our English. Fattorini, S., & Ulrich, W. (2012a). Drivers of species richness in European Tenebrionidae (Coleoptera). Acta Oecologica, 43,22–28. Conflict of interest The authors declare that they have no conflict of Fattorini, S., & Ulrich, W. (2012b). Spatial distributions of interest. European Tenebrionidae point to multiple postglacial coloni- zation trajectories. Biological Journal of the Linnean Society, London, 105,318–329. Fattorini, S., Sciotti, A., Tratzi, P., & Di Giulio, A. (2013a). Species References distribution, ecology, abundance, body size and phylogeny originate interrelated rarity patterns at regional scale. JournalofZoological Systematics and Evolutionary Research, 51,279–286. Aalbu, R. L., Triplehorn, C. A., Campbell, J. M., Brown, K. W., Somerby, Fattorini, S., Lo Monaco, R., Di Giulio, A., & Ulrich, W. (2013b). R. A., & Thomas, D. B. (2002). Family 106. Tenebrionidae Latreille Latitudinal trends in body length distributions of European darkling 1802. In R. H. Arnett Jr., M. C. Thomas, P. E. Skelley, & J. H. Frank beetles (Tenebrionidae). Acta Oecologica, 53,88–94. (Eds.), American Beetles. Volume 2. Polyphaga: Scarabaeoidea Felsenstein, J. (1985). Phylogenies and the comparative method. through Curculionoidea (pp. 463–509). Boca Raton: CRC. American Naturalist, 125,1–15. Baselga, A. (2008). Determinants of species richness, endemism and Ferrer, J. (2008). Contribución al conocimiento de los Asinini turnover in European longhorn beetles. Ecography, 31,263–271. iberobaleares. Segunda nota. Las Alphasida (Glabrasida) Cabrero-Sañudo, F. J. (2012). Composition and distribution patterns of del grupo Tricostatae Escalera 1922 (Coleoptera, species at a global biogeographic region scale: Biogeography of Tenebrionidae, Pimeliinae). Boletín Sociedad Entomológica Aphodiini dung beetles (Coleoptera, Scarabaeidae) based on species Aragonesa, 43,61–73. 224 S. Fattorini et al.

Ferrer, J. (2011). Contribución al conocimiento del Género Phylan Peat, J., Darvill, B., Ellis, J., & Goulson, D. (2005). Effects of climate on dejean, 1821, y descripción de una especie nueva del género intra- and interspecific size variation in bumble bees. Functional Heliopates Dejean, 1834 (Coleoptera, Tenebrionidae, Pedinini). Ecology, 19,145–151. Boletín Sociedad Entomológica Aragonesa, 49,75–82. Penev, L. (1996). Large-scale variation in carabid assemblages, with Hadley, N. F. (1994). Water relations of terrestrial arthropods. San special reference to the local fauna concept. Annales Zoologici Diego: Academic Press. Fennici, 33,49–63. Homburg, K., Schuldt, A., Drees, C., & Assmann, T. (2012). Broad-scale Pons, J., Bruvo, B., Petitpierre, E., Plohl, M., Ugarkovic, D., & Juan, C. geographic patterns in body size and hind wing development of (2004). Complex structural features of satellite DNA sequences in western Palaearctic carabid beetles (Coleoptera: Carabidae). the genus Pimelia (Coleoptera: Tenebrionidae): random differential Ecography, 36,166–177. amplification from a common ‘satellite DNA library’. Heredity, 92, Knouft, J. H. (2004). Latitudinal variation in the shape of the species body 418–427. size distribution: an analysis using freshwater fishes. Qecologia, Rangel, T.F.L., Diniz-Filho, J.A.F., Bini, L.M. (2010). SAM: a compre- 139,408–417. hensive application for Spatial Analysis in Macroecology Köhler, F. (1996) Zur Käferfauna (Col.) des Korretsberges und des Ecography, 33, 46–50. Michelberges im Mittelrheintal. Mitteilungen der Ryder, O. A. (1986). Species conservation and systematics: the dilemma Arbeitsgemeinschaft Rheinischer Koleopterologen (Bonn) 6, 3–36. of subspecies. Trends in Ecology and Evolution, 1,9–10. Krasnov, B., Ward, D., & Shenbrot, G. (1996). Body size and leg Soldati, F., & Soldati, L. (2006). Species delimitation using morpholog- length variation in several species of darkling beetles ical and molecular tools in the Asida (Polasida) jurinei Solier, 1836 (Coleoptera: Tenebrionidae) along a rainfall and altitudinal species-complex. Preliminary results. (Coleoptera: Tenebrionidae: gradient in the Negev Desert (Israel). Journal of Arid Tentyrinae). Cahiers Scientifiques Muséum Lyon, 10, 111–116. Environments, 34,477–489. Speight, M. R., Hunter, M. D., & Watt, A. D. (2008). Ecology of insects Levkaničová, Z. (2009). Molecular phylogeny of the superfamily (2nd ed.). Oxford: Wiley-Blackwell. Tenebrionoidea (Coleoptera: Cucujiformia). Ph.D. Thesis. Stevenson, R. D. (1985). Body size and limits to the daily range of body Olomouc: Faculty of Science, Department of Zoology and temperature in terrestrial ectotherms. American Naturalist, 125, Anthropology, Palacký University. 102–117. Löbl, I., & Smetana, A. (2008). Catalogue of palaearctic coleoptera. Stroscio, S., Baviera, C., Frati, F., Lo Paro, G., & Nardi, F. (2011). Deep Volume 5. Tenebrionoidea. Stenstrup: Apollo Books. genetic divergence in the darkling beetle Pimelia rugulosa Lomolino, M. V., Riddle, B. R., Whittaker, R. J., & Brown, J. H. (2010). (Coleoptera, Tenebrionidae) reflects Plio-Pleistocenic paleogeo- Biogeography (Forthth ed.). Sunderland: Sinauer. graphic history of Sicily. Journal of Zoological Systmatics and Marcuzzi, G. (1960). Rapporti tra equilibrio idrico e ambiente nei Evolutionary Research, 49,196–203. Coleotteri Tenebrionidi. Archivio Zoologico Italiano, 45,325–342. Trichas, A. (2008). The genus Dendarus Latreille, 1829 (Coleoptera, Meiri, S., Dayan, T., & Simberloff, D. (2005). Biogeographical patterns Tenebrionidae: Dendarini) in Greece (A systematic account of the in the Western Palearctic: the fasting-endurance hypothesis and the genus with description of a new species and four new systematic status of Murphy’srule.Journal of Biogeography, 32,369–375. combinations). In: S. E. Makarov, Dimitrijević,R.N.(Eds.), Murphy, E. L. (1985). Bergmann’s rule, seasonality and geographic Advances in arachnology and developmental biology (pp. 417– variation in body size of house sparrows. Evolution, 39,1327–1334. 462). Belgrade: SASA, Belgrade & UNESCO MAB Serbia. Olson, V. A., Davies, R. G., Orme, C. D. L., Thomas, G. H., Meiri, S., Ulrich, W., & Fiera, C. (2010). Environmental correlates of body size Blackburn, T. M., et al. (2009). Global biogeography and ecology of distributions of European springtails (Hexapoda: Collembola). body size in birds. Ecology Letters, 12,249–259. Global Ecology and Biogeography, 19,905–915.