What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae)

What determines a species’ geographical range?

Thermal biology and latitudinal range size relationships

in European diving beetles (Coleoptera: Dytiscidae)

Piero Calosi*, David T. Bilton, John I. Spicer, StephenC. Votier and AndrewAtfield

Marine Biology and Ecology Research Centre, Faculty of Science, University of Plymouth, Drake Circus,

Plymouth, Devon PL4 8AA, UK

Summary

1. The geographical range sizes of individual species vary considerably in extent, although the fac-

tors underlying this variation remain poorly understood, and could include a number of ecological

and evolutionary processes. A favoured explanation for range size variation is that this result from

differences in fundamental niche breadths, suggesting a key role for physiology in determining

range size, although to date empirical tests of these ideas remain limited.

2. Here we explore relationships between thermal physiology and biogeography, whilst control-

ling for possible differences in dispersal ability and phylogenetic relatedness, across 14 ecologically

similar congeners which differ in geographical range extent; European diving beetles of the genus

Deronectes Sharp (Coleoptera, Dytiscidae). Absolute upper and lower temperature tolerance and

acclimatory abilities are determined for populations of each species, following acclimation in the

laboratory.

3. Absolute thermal tolerance range is the best predictor of both species’ latitudinal range extent

and position, differences in dispersal ability (based on wing size) apparently being less important in

this group. In addition, species’ northern and southern range limits are related to their tolerance of

low and high temperatures respectively. In all cases, absolute temperature tolerances, rather than

acclimatory abilities are the best predictors of range parameters, whilst the use of independent con-

trasts suggested that species’ thermal acclimation abilities may also relate to biogeography,

although increased acclimatory ability does not appear to be associated with increased range size.

4. Our study is the first to provide empirical support for a relationship between thermal physiology

and range size variation in widespread and restricted species, conducted using the same experimen-

tal design, within a phylogenetically and ecologically controlled framework.

Key-words: biogeography, macroecology ⁄macrophysiology, niche-breadth hypothesis, rarity,

thermal tolerance

Introduction

It has long been recognized that the geographical ranges of

individual species vary enormously in extent, most taxa being

endemic to relatively small areas, whilst comparatively few

are widespread (Darwin 1859; Darlington 1957; MacArthur

1972; Gaston 1996, 2003). Within clades, species-range size

distributions tend to be unimodal, with a strong right or posi-

tive skew, a pattern that appears to be almost universal,

across a wide range of taxa and habitats (Gaston & Black-

burn 2000; Gaston 2003). Despite our increasing knowledge

of macroecological patterns, the factors determining the

relative geographical range sizes of organisms are still poorly

understood, with range size variation potentially resulting

from a number of ecological and evolutionary processes (see

Gaston 2003). These include interspecific differences in evo-

lutionary age (e.g. Taylor &Gotelli 1994), population genetic

structure and levels of gene flow (e.g. Kirkpatrick & Barton

1997; Gaston 2003), dispersal ability (DA) (e.g. Juliano 1983;

Bohning-Gaese et al. 2006; Rundle et al. 2007a) and

fundamental niche breadth (Brown 1984; Gaston & Spicer

2001). The last class of hypotheses proposes that species with

broader fundamental niches will tend to achieve greater local

densities, survive in more places, and so occupy wider

geographical areas than narrow-niched relatives (Gaston &

Spicer 2001) – the geographical range of a species being*Correspondence author. E-mail: [email protected]

Journal of Animal Ecology 2010, 79, 194–204 doi: 10.1111/j.1365-2656.2009.01611.x

� 2009TheAuthors. Journal compilation� 2009 British Ecological Society

considered as a spatial reflection of its ecological niche

(Lomolino, Riddle & Brown 2006).

In terms of fundamental niche breadth, variation in physi-

ological traits is generally considered to play a pivotal role

(Spicer & Gaston 1999; Gaston & Spicer 2001), predicting

that widespread taxa will have broader ranges of physiologi-

cal tolerance and plasticity than their restricted relatives (see

also Brattstrom 1968, 1970; Calosi, Bilton & Spicer 2008b;

Gaston et al. in press). Furthermore, a favoured explanation

for the generally observed increase in latitudinal range extent

with latitude in the Northern Hemisphere (Rapoport’s Rule)

relates to differences in physiological tolerance (Stevens

1989; Gaston, Blackburn & Spicer 1998; Compton et al.

2007). This ‘climatic variability hypothesis’ suggests that

higher latitude species survive over larger areas due to

broader thermal tolerance, selected for as a result of greater

temporal climatic variation at higher latitudes. Despite some

evidence suggesting that species’ physiological tolerances

relate to geographical range extent (e.g. Janzen 1967; Gaston

&Chown 1999; Addo-Bediako, Chown&Gaston 2000; Gas-

ton & Spicer 2001; Hoffmann, Anderson &Hallas 2002; Still-

man 2002; Ghalambor et al. 2006; Gaston 2009; but see also

van Herrewege & David 1997), there have been few empirical

attempts to explore the relationship between physiological

traits and variation in species’ geographical distribution (see

Huey & Slatkin 1976; Adolph & Porter 1993; Buckley &

Roughgarden 2005; Bernardo et al. 2007), and there remains

a need for data from groups of ecologically similar, related

species if we are to better understand the relationship

between species’ physiology and biogeography (see for exam-

ple Thompson,Gaston & Band 1999).

Environmental temperatures have long been seen as criti-

cal in determining species’ distributions (e.g. Andrewartha &

Birch 1954; Merriam 1984), and an organism’s thermal toler-

ance and acclimatory abilities are critical aspects of its physi-

ological niche (Spicer & Gaston 1999). In biogeographical

terms, many past studies have noted coincidences between

geographic range boundaries and temperature isotherms,

across a range of organisms (Salisbury 1926; Caughley et al.

1987; Root 1988; Iversen 1994). As well as absolute thermal

tolerance, an organism’s thermal plasticity may be important

in shaping where it can and cannot occur (see Janzen 1967;

Brattstrom 1968, 1970; Gaston & Chown 1999; Klok &

Chown 2003; Chown & Terblanche 2007), as acclimatory

abilities give an organism the potential to express a wider

thermal tolerance range.

The ecological impacts of recent climatic changes are

becoming increasing well documented, and include apparent

range expansions and shifts, genetic changes in natural popu-

lations and increased population extinction rates (e.g. Parme-

san et al. 1999; Hill et al. 2002; Walther et al. 2002; Balanya

et al. 2006). Despite this, there are few demonstrated exam-

ples where a species’ apparent response to climatic changes

has been linked to a specific physiological or evolutionary

mechanism (e.g. Crozier & Dwyer 2006; Portner & Knust

2007; Kearney et al. 2009). Attempts to elucidate the

mechanisms behind range size variation need to consider

both current and historical biogeography; restricted and

widespread species are not evenly distributed across the

globe, and species’ ranges are themselves dynamic. In the

western Palaearctic, narrow-range endemic species are con-

centrated in lands around the Mediterranean, which are also

widely recognized as having functioned as refugia for many

temperate taxa during Quaternary glacial cycles (e.g. Taber-

let et al. 1998; Hewitt 2004; Willis & Niklas 2004). The wide-

spread species of present-day Europe have become

widespread as a result of range expansion in the Holocene,

and often belong to clades dominated by restricted southern

endemics (e.g. Thompson 2005). In this context, why have

some species been able to expand widely outside their Pleisto-

cene refugia, whilst others remain largely restricted to these

areas? Such questions apply not only to Europe, but to any

areas where the extant ranges of organisms have been shaped

by Quaternary climate shifts (Nilsson 1983), and may shed

important light on the likely responses of widespread and

restricted taxa to current climatic changes.

Here, we explore the relationships between thermal physi-

ology and biogeography within a well-defined taxonomic

assemblage of ecologically similar species; European diving

beetles of the genus Deronectes Sharp (Coleoptera, Dytisci-

dae). Species of Deronectes occur in fast-flowing streams at

intermediate elevations across the Palaearctic, with greatest

diversity in the Mediterranean region (Franciscolo 1979;

Millan & Ribera 2001; Ribera & Vogler 2004). The phyloge-

netic inter-relationships of European species are well docu-

mented based on mitochondrial cytochrome oxidase and 16s

ribosomal DNA sequences (Ribera, Barraclough & Vogler

2001; Ribera & Vogler 2004). Most European species belong

to a single clade, with the exception of the Deronectes latus

group, which is more closely related to eastern Mediterra-

nean taxa (Fery & Hosseinie 1998; Ribera et al. 2001). Dero-

nectes species are generalist predators, feeding on a range of

small aquatic invertebrates, and having similar general ecolo-

gies across their geographical ranges, although differing

markedly in latitudinal range size. Whilst inhabiting a rela-

tively thermally buffered aquatic medium (see Giller &

Malmqvist 1998), in-stream temperatures experienced by

these beetles vary both seasonally and latitudinally. In sites

occupied by Deronectes in Andalucia, Spain, for example,

water temperatures can vary between 6 and 30 �C annually

(A. Millan, P. Abellan & D. Sanchez-Fernandez, personal

communication), whilst in southern England, temperatures

in sites suitable for D. latus Stephens can fluctuate between 2

and 25 �C (D. T. Bilton, personal observation; Hildrew &

Edington 1979). Widespread pan-European species of

Deronectes experience greater macroclimatic variability than

restricted southern endemics, and it is likely that widespread

species also live under a greater range of microclimates, as

species inhabit the same suite of microhabitats across their

ranges (Sutton 1953).

We investigate the relationship between thermal physiol-

ogy and latitudinal range extent and position amongst 14

species of Deronectes, whilst controlling for possible differ-

ences in dispersal ability, and the effects of phylogenetic

Species’ geographical range determinants 195

� 2009 TheAuthors. Journal compilation� 2009 British Ecological Society, Journal of Animal Ecology, 79, 194–204

relationship (Harvey & Pagel 1991; Garland, Bennett & Rez-

ende 2005). In addition, we explore the relationships between

species’ thermal biology and southern and northern range

limits. Our study represents the most extensive empirical

exploration to date of the relationship between thermal phys-

iology and range size variation in widespread and restricted

congeners, conducted using the same experimental design,

examining relatively large numbers of individuals of both

rare and common species, within a phylogenetically and eco-

logically controlled framework.

Materials andmethods

SPECIMEN COLLECTION, MAINTENANCE AND

PREPARATION

AdultDeronectes were collected during spring and summer 2006 (see

Appendix S1, Supporting Information) standardizing as much as

possible for season of collection, working a D-Framed pond net

(1 mm mesh, dimensions 20 · 25 cm) along stream banks. We stud-

ied adults as these are the life-history stage of longest duration

(‡1 year), readily collected from the field, whilst larvae are short lived

(c. 1–2 months), rarely collected due to their interstitial habits, and

morphologically intractable. In addition, it is the adult stage which

overwinters, and survives periodic droughts (Nilsson & Holmen

1995), making adult thermal tolerance most relevant here. All indi-

viduals collected were early post-teneral adults, minimizing any pos-

sible confounding effects due to age variation (Bowler & Terblanche

2008). All species were collected as close as possible to the central

point of their latitudinal ranges, to avoid the possible confounding

effects of local adaptation in range edge populations, and to ensure

data were comparable for each species (Thompson et al. 1999). Given

the largely allopatric occurrence of many species, and differences in

the latitudinal position of their ranges, it is impossible to sample all

taxa from the same latitude. Data on species’ geographical distribu-

tions were taken fromFery & Brancucci (1997) and Fery &Hosseinie

(1998). Latitudinal range extents were calculated as the difference (in

degrees latitude) between northern and southern distributional limits

(Gaston 1994), and latitudinal range central points determined as the

mid-point of each species’ latitudinal range extent (see Appendix S1,

Supporting Information).

After collection individuals were transported to the laboratory in

plastic containers (vol. = 1 L) filled with damp, aquatic vegetation,

kept within thermally insulated bags (Thermos�, Rolling Meadows,

IL, USA) to reduce temperature variation in the containers. In the

laboratory, specimens were maintained in aerated artificial pond

water [APW, pH 7Æ5, acidified using HCl (ASTM 1980)], distributed

between a number of aquaria (vol. = 5 L, maximum 20 individuals

per aquarium) in a 12 : 12 h L ⁄D regime, and fed chironomid larvae

ad libitum. Individuals fed, and mated in our treatments, suggesting

they were functioning in a normal manner. Aquaria were sealed with

Cling-film� to reduce evaporation and prevent individuals escaping.

All the work was conducted in computer-controlled constant temper-

ature rooms. The maximum water temperature fluctuation amongst

all aquaria over the acclimation period was 0Æ6 �C, measured with a

maximum–minimum thermometer (Jumbo Thermometer Oregon

Scientific� model EM899 ± 0Æ1 �C; Oregon Scientific�, Portland,

OR, USA). In an attempt to avoid possible confounding effects of

individuals’ recent thermal history, specimens weremaintained under

identical, constant conditions in the laboratory prior to experiments

(e.g. Sokolova & Portner 2003), which is likely to minimize prior

acclimatization effects on individuals. Each species was divided

haphazardly into two equal groups, acclimated at 14Æ5 or 20Æ5 �Crespectively and specimens were maintained in the laboratory for

7 days at these two temperatures before experiments were conducted

(Hoffmann & Watson 1993; Klok & Chown 2003; Terblanche &

Chown 2006). Temperatures were chosen as being within the range

experienced by Deronectes adults in the field (D. T. Bilton, personal

observation; S. Fenoglio, A. Millan, P. Abellan & D. Sanchez-

Fernandez, personal communication), and were the same for all spe-

cies studied to compare relative acclimation abilities of taxa. During

acclimation the use of extreme temperatures was avoided, as these

could have potentially acted (at least for certain species) as deleteri-

ous (pejus) temperatures (see Portner 2002; Woods & Harrison

2002), suggesting acclimation was probably not stressful, and indeed

nomortality occurred during acclimation. After acclimation, individ-

uals from each acclimation-temperature group were further haphaz-

ardly assigned to two equal subgroups: used to measure tolerance to

heat and cold respectively for individuals of each species kept at 14Æ5or 20Æ5 �C.

THERMAL LIMITS AND ACCLIMATORY ABIL ITY OF

DERONECTES SPECIES

To define species’ thermal biology we employed upper and lower

lethal thermal limits [defined as upper thermal limit (UTL) and lower

thermal limit (LTL) subsequently], as these proved the most reliable,

repeatable measure of thermal tolerance in diving beetles. Lethal

limits were favoured amongst the various end-points which could be

identified in thermal tolerance experiments, as they showed the low-

est variance (see Lutterschmidt & Hutchison 1997a,b; Calosi et al.

2008a); however, the use of sublethal end-points (e.g. paralysis) did

not change results.

Experiments commenced at the temperature to which individuals

of a given subgroup had been acclimated. Thermal tolerance tests

relied on a dynamic method, and were carried out in air in generic,

24-well (diameter = 12 mm, depth = 18 mm) plastic culture plates

(Corning Ltd, Sunderland, UK), placed in a computer-controlled

water bath (Grant LTC 6–30), heated and cooled, via a ramping pro-

gram (±1 �C min)1) using the Grant Coolwise Software [Grant

Instruments (Cambridge) Ltd, Herts, UK]. Experimental ramping

rate and equilibration temperature can influence the outcome of ther-

mal tolerance tests (Terblanche et al. 2007; Chown et al. 2009), and

selecting an ecologically relevant ramping rate is difficult when com-

prehensive environmental data are lacking. Consequently, we

employed an identical ramping rate, to allow comparisons amongst

taxa, and with previous studies (Lutterschmidt & Hutchison

1997a,b).

Individuals were introduced, one per well, to a maximum of 12

individuals at any one time, with two investigators working

together, for accurate determination of thermal tolerance limits.

The actual temperature within each well was measured directly

using a calibrated digital thermometer (Omega� HH11; Omega

Engineering Inc., Stamford, CT, USA) equipped with an Omega�

‘precision fine wire thermocouple’ (type K – dia. ⁄ ga. 0Æ010 Teflon).

Individuals were removed from their acclimation aquaria, quickly

but carefully dried on absorbent paper and placed into a clean, dry,

well. To avoid escape, well plates were covered with their plastic lids

between addition of individuals. Once the experiment started, the

lid was removed to allow full aeration and avoid the build-up of

water vapour.

Thermal range (TR) was calculated as the difference betweenmean

UTL at 20Æ5 �C and LTL at 14Æ5 �C, as these are likely to represent

196 P. Calosi et al.

� 2009 TheAuthors. Journal compilation� 2009British Ecological Society, Journal of Animal Ecology, 79, 194–204

the most ecologically realistic measures of a species’ tolerance of high

and low temperatures (as they follow high and low acclimation

temperatures, respectively – see Calosi et al. 2008b – and, overall,

species showed higher tolerance to heat and cold when acclimated at

these temperatures). Upper and lower thermal tolerance acclimatory

abilities (DUTL and DLTL) were estimated as the absolute difference

between the thermal limits (for high or low temperatures respectively)

measured at the two acclimation temperatures (Stillman 2003). A

positive value for either DUTL or DLTL indicates a positive ability

of a species to increase its mean UTL or mean LTL, following

acclimation at a higher or lower temperature. After the experiments

individuals were weighed (to ±0Æ001 g) using a Sartorius 1204 MP2

balance (Sartorius Ltd, Epsom, UK).

DISPERSAL ABIL ITY

Obtaining accurate estimates of species’ relative dispersal ability

(DA) is difficult (see Bilton, Freeland & Okamura 2001), as dispersal

itself is an emergent trait, influenced by numerous morphological,

physiological and ecological factors (Rundle, Bilton & Foggo

2007b). For aerial dispersers such as Deronectes species, however,

wing size is an obvious feature which has been suggested to correlate

with relative DA (e.g. Rundle et al. 2007a). This is particularly likely

to hold in comparisons of closely related, otherwise similar, taxa, and

the use of wing size as a surrogate of relative DA was adopted here.

We specifically use wing length ⁄ body length ratio, as this is likely to

provide a good comparative measure of the relative DA of diving

beetle species (see Rundle et al. 2007a): other possible surrogates of

DA (wing length, wing area ⁄ body mass ratio) were also explored,

and gave the same results as those presented here. Individuals whose

wings were to be examined were first photographed intact under a

LeicaMZ8 stereomicroscope (·50mag) using a Nikon Coolpix 4500.

The right wing was removed from 10 individuals of each species,

digested in 10% potassium hydroxide for 15 min to increase

flexibility, before being teased open and mounted in lactic acid

solution (DL-lactic acid 85% w ⁄w syrup – Sigma Chemical Co., St

Louis, MO, USA) on a microscope slide. Disarticulated wings were

examined and photographed as described above, and wing

length estimated using UTHSCA Image Tool Version 3.0. Body

length of each individual was measured from the front of the prono-

tum to the tip of the elytra (to avoid measurement error due to

contraction of head into pronotum) using the same photomicro-

scopic approach.

STATIST ICAL ANALYSES

Species’ body mass differed significantly amongst Deronectes

(F13, 712 = 90Æ282; n = 726; P < 0Æ0001), and was therefore consid-ered as a covariate in subsequent analyses. The number of individuals

studied ranged from 26 in Deronectes angusi Fery and Brancucci to

92 inD. hispanicusRosenhauer.No significant correlation was found

between the number of individuals of each species examined and any

physiological, ecological or biogeographical trait (Pearson correla-

tion minimum Z12 = 1Æ148; P = 0Æ251), indicating that interspecificdifferences in sample size did not influence results.Mean bodymasses

(±SE) and the number of individuals tested for each species are given

inAppendix S2, Supporting Information.

Differences in mean UTL and mean LTL among species were

first analysed separately using an ancova, including body mass as a

covariate, whilst differences in mean DA among species were anal-

ysed using an ANOVA. We investigated factors influencing varia-

tion in latitudinal range extent and position, and both northern

and southern range limits using a series of multiple regression

models. Akaike’s Information Criteria (AIC) was used to select the

best supported models, an approach which reduces problems asso-

ciated with multiple testing and co-linearity of explanatory vari-

ables (Burnham & Anderson 2002). In each analysis, models were

constructed using all combinations of experimental variables, and

the five best models presented in the results. The single best sup-

ported model for each analysis was selected on the basis of the

AIC weights, calculated to evaluate the relative likelihood of a

model, given the data and the fitted model, scaled to one (Burn-

ham & Anderson 2002). Model selection was performed using both

raw data and independent contrasts (Felsenstein 1985) derived

from mtDNA based phylogenies (Ribera et al. 2001; Ribera & Vo-

gler 2004). Contrasts were produced using the CRUNCH algo-

rithm of the CAIC software package (Purvis & Rambaut 1995),

and regressions of contrast scores forced through the origin (Gar-

land, Harvey & Ives 1992).

Species’ southern range limits were normally distributed, whilst

latitudinal range extent and central point were normalized following

log10 transformation. In the case of northern range limits, data were

normalized following double log10 transformation. Normality in all

cases was assessed via Shapiro–Wilks test; P > 0Æ05. All statistical

analyses were conducted using JMP IN� version 5.1, except for mul-

tiple regression models, which were run in R v.2.5.1 (R Development

Core Team, 2007) and SPSS v.15.0.

Results

THERMAL LIMITS AND ACCLIMATORY ABIL IT IES OF

DERONECTES SPECIES

Upper and lower thermal limits differed significantly between

species of Deronectes at all acclimations tested (ANCOVA

minimum F13,173 = 8Æ797; P < 0Æ0001 – see Appendix S2,

Supporting Information for species’ values). Mean body

masses ranged between 5Æ37 mg in D. platynotus platynotus

Germar and 10Æ54 mg in D. opatrinus Germar (see Appen-

dix S2, Supporting Information), but did not affect species’

ability to tolerate either high or low temperatures (ANCOVA

maximum F13,160 = 0Æ623; P = 0Æ431). Given that body

mass did not influence thermal tolerance, we explored

differences between species’ performances (excluding body

mass from the analysis) via one-way ANOVAs, which

showed that species differ significantly in both UTL and LTL

(minimum F13,173 = 13Æ125; P < 0Æ0001). ANOVAs were

employed in conjunction with Tukey–Kramer tests. These

analyses were carried out separately on UTL at 20Æ5 �C and

LTL at 14Æ5 �C (see Fig. 1), focusing on these acclimations as

these values are used in further analyses (seeMethods).

Mean UTL ranged from 42Æ6 �C in D. semirufus Germar

to 46Æ9 �C in D. latus, both following 20Æ5 �C acclimation

(Appendix S2, Supporting Information; Fig. 1a), and mean

LTL ranged from )3Æ4 �C in D. algibensis Fery and Fresne-

da, to )10Æ0 �C in D. latus, both following acclimation at

14Æ5 �C (Appendix S2, Supporting Information; Fig. 1b).

Furthermore, phylogenetically independent contrasts reveal

that the ability to tolerate heat and cold are significantly

negatively correlated across the genus (Pearson correlation

Species’ geographical range determinants 197

� 2009 TheAuthors. Journal compilation� 2009 British Ecological Society, Journal of Animal Ecology, 79, 194–204

Z11 = 3Æ779; P = 0Æ0004). Mean DUTL ranged from

)1Æ13 �C in D. wewalkai Fery and Fresneda to 2Æ02 �CD. latus, whilst mean DLTL ranged from )1Æ99 �C in

D. opatrinus to 1Æ42 �C in D. platynotus mazzoldi Fery and

Brancucci (see Appendix S2, Supporting Information).

Phylogenetically independent contrasts reveal that the

ability to acclimate to heat and cold are significantly posi-

tively correlated across the genus (Pearson correlation

Z11 = 7Æ679; P < 0Æ000001). Wing length ⁄body length

ratio differed significantly amongst taxa (ANOVA

F13,140 = 74Æ527; P < 0Æ0001), ranging from 1Æ00 in

D. angusi to 1Æ30 in D. fairmairei Leprieur (see Appendix S2,

Supporting Information).

THERMAL BIOLOGY AND RANGE SIZE AND POSIT ION

The best supportedmodels examining range size and position

always contained TR, which was the only parameter to be

significant in all cases (Table 1). Model evidence suggested

that latitudinal range extent was strongly positively related to

a species’ TR, and this was the only parameter included in

the best supported model (TR slope = 0Æ178, SE = 0Æ061;Fig. 2a). After controlling for phylogeny, the best predictor

for latitudinal range extent was still TR; additionally in some

models range size was found to be significantly negatively

related to DLTL and ⁄or positively to DA. In one case, a sig-

nificant positive relationship between latitudinal range extent

and DUTLwas suggested, although this model had relatively

low support (see Table 1). The best selected model included

all parameters considered, however only TR (slope = 0Æ281,

SE = 0Æ012) and DLTL (slope = )0Æ276, SE = 0Æ104), hadsignificant slopes.

Latitudinal range central point was always significantly

positively related to TR, species with more northerly ranges

possessing broader TRs, whilst in one model latitudinal

range central point was also negatively related to DLTL(Table 1). The best supported model included TR and DA,

but only TR had a significant slope (TR slope = 0Æ016,SE = 0Æ005; Fig. 2b). After controlling for phylogeny, TR

again emerged as the strongest predictor, being positively

related to range position in all the best selected models

(Table 1). In some models range position also appeared to be

significantly negatively related to DLTL, and in three cases to

DUTL (positively) and in one case to body mass (negatively),

although most of these models had relatively weak support.

The best supported model contained all parameters consid-

ered, but only TR (slope = 0Æ022, SE = 0Æ001), DLTL (slo-

pe = )0Æ019, SE = 0Æ007) and body mass (slope = )0Æ005,SE = 0Æ002) had a significant slope.

THERMAL BIOLOGY AND RANGE LIMITS

All best supported models for southern range limit contained

UTL, which was the only significant parameter in all cases

(Table 2). In general, species ofDeronecteswith greater toler-

ance to high temperatures showed lower southern range lim-

its. The best supported model explaining variation in

southern range limit includedUTL,DUTLandDA (Table 2),

but only UTL showed a significant slope (UTL slo-

pe = )2Æ645, SE = 0Æ947; Fig. 3a). Following phylogenetic

transformation both UTL and DUTL appeared as strong

predictors of southern range limit. Again, species with higher

UTL showed lower southern limits, whilst species with higher

DUTL had higher southern limits. The best selected model

included all parameters, but only UTL andDUTLhad signif-

icant slopes (Table 2; UTL slope = )0Æ956, SE = 0Æ261;DUTL slope = 0Æ503, SE = 0Æ174).Finally, species with the greatest tolerance to low tempera-

tures had the highest northern range limits. LTL was always

significant if present (Table 2), and was the only parameter

included in the best selected model, being negatively related

to northern range limit (LTL slope = )6Æ661, SE = 1Æ593;Fig. 3b). Although this may appear counter intuitive, LTL

values are negative, indicating that those species which are

most tolerant to cold possess the highest northern limits.

Following phylogenetic correction, LTL again emerged as

the strongest predictor of northern range limits. Addition-

ally, in most models, DLTL appeared to be significantly

negatively related to northern range limits, as was body mass

in two cases. Indeed the best selected model included LTL

(slope = )9Æ582, SE = 0Æ776), DLTL (slope = )5Æ473,SE = 0Æ659) and bodymass (slope = )7Æ753, SE = 1Æ235).

Discussion

Thermal tolerance range represents an integrative estimate of

absolute thermal niche breadth inDeronectes, and appears to

50

11,2 2 22,3 2,3,4 2,3,4 2,3,4 4 3,4,5 4,5

5 5 5

48

46

44

42

40

UT

L (º

C)

LTL

(ºC

)

38

36

0

(b)

(a)

–2

–4

–6

–8

–10

–12

–14

1 1 1 1 1,2 1,2,3 1,2,3 1,2,3 1,2,3,41,2,3,43,4 2,3,4,5

4,55

Species

Latus

Latus

Fairmaire

i

Fairmaire

i

Algibensis

Algibensis

Opatrinus

Opatrinus

Hispanicu

s

Hispanicu

s

Depress

icollis

Depress

icollis

Moestus

Moestus

Platynotus m

azzoldi

Platynotus m

azzoldi

Platynotus p

latynotus

Platynotus p

latynotus

Angusi

Angusi

Semirufus

Semirufus

Wew

alkai

Wew

alkai

Bicosta

tus

Bicosta

tus

Aubei aubei

Aubei aubei

Fig. 1. Thermal performance of Deronectes species (a) upper thermal

limits (UTLs) measured following 20Æ5 �C acclimation; (b) lower

thermal limits (LTLs) measured following 14Æ5 �C acclimation. Bars

represent species’ mean thermal limits (�C;±SE). Different numbers

indicate significant differences between means (P < 0Æ05). Sample

sizes are given in Appendix S2, Supporting Information.

198 P. Calosi et al.

� 2009 TheAuthors. Journal compilation� 2009British Ecological Society, Journal of Animal Ecology, 79, 194–204

be the best predictor of both their latitudinal range extent

and position. In Deronectes, widespread, more northerly dis-

tributed species possessed broader thermal tolerance win-

dows than their restricted, more southern relatives. Although

broader thermal tolerance windows may have shaped range

size evolution in these taxa, or vice versa, we favour the for-

mer explanation here, particularly as our data are based on

studies of single, central populations. Local adaptation may

lead to greater inter-population variation in thermal physiol-

ogy in a species with a large geographical range, and as a con-

sequence, some inter-populational differences in thermal

physiology may be expected, particularly for the most wide-

spread species of Deronectes, as has been reported in some

other insect species (e.g. Garland & Adolph 1991; Huey, Par-

tridge & Fowler 1991; Hoffmann & Watson 1993; Klok &

Chown 2003; Terblanche et al. 2006). Whilst gene flow could

result in broader thermal tolerance windows within central

populations of such species, through the admixture of locally

adapted genotypes, we feel this is unlikely to be the case here.

Species of Deronectes are patchily distributed in suitable

stream systems throughout their ranges, and, as with most

lotic Coleoptera, show relatively strong spatial genetic struc-

ture (e.g. Ribera et al. 2001; Ribera, Bilton & Vogler 2003),

suggesting gene flow levels are relatively low in these taxa.

Within the genus, more northerly distributed species are

also those which have the largest geographical ranges; latitu-

dinal range extent and latitudinal range central point

being positively related in Deronectes (Pearson correlation

analyses: untransformed data Z12 = 2Æ275; P < 0Æ0000001;phylogenetically independent contrasts Z11 = 59Æ182;P = 0Æ023). These findings lend some support to Stevens

(1989) ideas regarding the factors underlying the relationship

between latitudinal range extent and position.

In conventional multiple regression models, species’ accli-

matory abilities were not significant predictors of latitudinal

range extent, and therefore results do not support Gaston &

Spicer’s (2001) prediction that widespread species should

have higher acclimation abilities than their restricted rela-

tives. In many insects, acclimatory responses across tempera-

ture gradients are known to be nonlinear (e.g. Terblanche

et al. 2006), and as a consequence results such as ours, which

examine acclimation to the same two temperatures across a

range of taxa, should be interpreted with some caution, as

individual species may differ in the thermal windows over

which they can effectively acclimate. It also should be

acknowledged that the length of the experimental exposure

window can influence absolute estimates of critical thermal

limits (Terblanche et al. 2007; Chown et al. 2009). Assess-

ments of acclimatory ability which rely on different experi-

mental starting temperatures, as employed here, may be

influenced by these effects, although such issues are unlikely

to alter conclusions made from broad scale interspecific com-

parisons (Terblanche et al. 2007). In general,Deronectes spe-

cies appeared to have limited acclimatory ability of either

UTL or LTL, at least over the range of temperatures

employed in our study and using the current experimental

Table 1. Model selection to estimate factors influencing latitudinal range extent and latitudinal range central point inDeronectes species

Model np AIC DAIC AICweight

Latitudinal range extent

TR 2 )23Æ112 0Æ000 0Æ334TR + BM 3 )22Æ100 1Æ012 0Æ202TR + DLTL 3 )22Æ013 1Æ099 0Æ193TR + DA 3 )21Æ337 1Æ774 0Æ138TR + DUTL 3 )21Æ277 1Æ834 0Æ134

Latitudinal range extent (independent contrasts)

TR + DLTL + DUTL + BM + DA 5 )106Æ226 0Æ000 0Æ324TR + DLTL + BM + DA 4 )105Æ659 0Æ566 0Æ244TR + DLTL + DA 3 )105Æ087 1Æ138 0Æ183TR + DLTL + DUTL + DA 4 )104Æ728 1Æ498 0Æ153TR + DLTL + DUTL 3 )103Æ805 2Æ421 0Æ096

Latitudinal range central point

TR + DA 3 )92Æ940 0Æ000 0Æ270TR + DLTL + DUTL + BM 5 )92Æ848 0Æ092 0Æ258TR + DUTL + DA 4 )91Æ989 0Æ952 0Æ168TR + DLTL + DUTL + BM + DA 6 )91Æ893 1Æ048 0Æ160TR 2 )91Æ690 1Æ251 0Æ144

Latitudinal range central point (independent contrasts)

TR + DLTL + DUTL + BM + DA 5 )170Æ922 0Æ000 0Æ583TR + DLTL + DUTL + BM 4 )169Æ224 1Æ698 0Æ250TR + DLTL + DUTL 3 )166Æ800 4Æ122 0Æ074TR + DLTL + BM 3 )166Æ244 4Æ678 0Æ056TR + DLTL + DUTL+DA 4 )165Æ367 5Æ555 0Æ036

In each case thermal range (TR), acclimatory ability of upper and lower thermal tolerances (DUTL&DLTL respectively), bodymass (BM) and

dispersal ability (DA) (measured asmeanwing length ⁄ body length ratio) were included as independent variables. np = number of parameters;

AIC = Akaike’s Information Criteria. AICweight represents the likelihood of the model given the data. Parameters with a significant slope are

highlighted in bold.

Species’ geographical range determinants 199

� 2009 TheAuthors. Journal compilation� 2009 British Ecological Society, Journal of Animal Ecology, 79, 194–204

protocol (Calosi et al. 2008b). Analyses of independent con-

trasts data revealed an apparent negative relationship

betweenDLTL and both latitudinal range extent and latitudi-

nal range central point in Deronectes, suggesting that species

with large, northerly ranges have poor acclimatory abilities

at low temperatures. Whilst such a result may point to an

evolutionary trade-off between thermal limits and their accli-

mation abilities (Janzen 1967; Stillman 2003; Somero 2005;

Tewksbury, Huey & Deutsch 2008 and references therein),

no evidence of this has been found with LTLs in Deronectes

(see Chown&Terblanche 2007; Calosi et al. 2008b).

On the other hand, the fact that the ability to tolerate heat

and cold are significantly negatively correlated across the

genus may suggest a trade-off in the evolution of high and

low temperature tolerance. Intraspecific differences in upper

and lower thermal limits may not be uncommon in insects, as

the physiological mechanisms underpinning upper and lower

thermal tolerances are decoupled (e.g. Hoffmann et al. 2002;

Chown & Nicolson 2004; Klok, Sinclair & Chown 2004;

Terblanche et al. 2005), and apparent evolutionary trade-offs

in thermal adaptation have been reported elsewhere (e.g.

Bennett & Lenski 1993; Stillman 2003; Dixon et al. 2009; but

see also Huey & Kingsolver 1993), and may be important in

setting the limits of species’ distributions (see Portner et al.

2006; Chown & Terblanche 2007 and references therein). In

our study, the most widespread species, D. latus, possesses

the greatest tolerance of both high and low temperatures,

contrary to the trend observed above. It seems likely that the

wide thermal window of this species has been important in

shaping its distribution, especially when one compares the

performance of latuswith its very close relativeD. angusi (see

Ribera & Vogler 2004), which is restricted to northern Iberia,

and shows more limited tolerance of both high and low ther-

mal extremes.

Possible differences in relative DA do not appear to be

strongly related to biogeographical parameters in our analy-

ses. Whilst DA appears in a number of our best supported

models (see Tables 1 and 2), it only has a significant slope in

relation to latitudinal range extent, and then with a relatively

high standard error (see Results). Such findings contrast with

a number of studies which have suggested a primary role for

dispersal in shaping the range sizes of species within clades,

across a number of taxa (Juliano 1983; Bohning-Gaese et al.

2006; Rundle et al. 2007a). Whilst we have no information on

actual dispersal distances in these beetles, available data

point to a limited role of interspecific differences in DA in

shaping biogeography, particularly given the strong relation-

ship with thermal biology demonstrated here. Species of

Deronectes may simply be too similar in their relative dis-

persal abilities for such differences to be significant in shaping

their potential ranges.

Mean UTL ofDeronectes species ranged between 42Æ6 and46Æ9 �C, a total of 4Æ3 �C, whilst mean LTL ranged over

6Æ6 �C, from )3Æ4 to )10Æ0 �C. In both cases, lethal limits fall

well within the temperature interval reported for other tem-

perate insects living at similar latitudes (Addo-Bediako et al.

2000; Chown & Nicolson 2004). However, compared to

many temperate insects (see Addo-Bediako et al. 2000;

Chown & Nicolson 2004) it would appear that Deronectes

are not particularly cold hardy, something also observed in

Agabus species (see Calosi et al. 2008b), which possess similar

thermal limits, despite being up to eight times heavier. In

both conventional and independent contrast regression

models, absolute heat and cold tolerance in these insects

appear to be related to the position of their southern and

northern range limits respectively. Such findings are in gen-

eral agreement with data from a range of taxa (e.g. Addo-

Bediako et al. 2000; Ghalambor et al. 2006) but contrast with

Huey et al. (2009), who found that low latitude forest lizards

had the lowest CTMax values. Also in Deronectes, the use of

independent contrasts suggests additional relationships

between acclimatory abilities and body mass and range

boundaries. Low-latitude southern range boundaries are

apparently associated with a weaker ability to acclimate to

high temperatures, whilst higher latitude northern bound-

aries are associated with poorer acclimation to cold, and

smaller body size. As with range size and position, whilst

such findings may point to evolutionary trade-offs between

thermal limits and their acclimation abilities, this is appar-

ently not the case inDeronectes (see Calosi et al. 2008b), mak-

ing interpretation of these results difficult in the absence of

(a)

(b)

Fig. 2. Relationship between thermal tolerance range (�C) and: (a)log-transformed latitudinal range extent (log10 LRE–� latitude) and

(b) log-transformed latitudinal range central point (log10 LRCP–�latitude) in Deronectes species. Symbols represent individual species’

as follows: algibensis (ALG), angusi (ANG), aubei aubei (AUB), bico-

status (BIC), depressicollis (DEP), fairmairei (FAI), hispanicus (HIS),

latus (LAT), moestus (MOE), opatrinus (OPA), platynotus mazzoldi

(MAZ), platynotus platynotus (PLA), semirufus (SEM), wewalkai

(WEW). Lines represent the tendency of data points, where a signifi-

cant relationship was found.

200 P. Calosi et al.

� 2009 TheAuthors. Journal compilation� 2009British Ecological Society, Journal of Animal Ecology, 79, 194–204

further data on the mechanisms underlying thermal tolerance

and acclimation in these beetles. The relationships between

range boundaries and temperature tolerances occur despite

the fact that in the Mediterranean region species may be

expected to have ‘hard’ southern range boundaries, defined

by barriers to dispersal for temperate freshwater taxa, such

as the northern shore of the Mediterranean sea itself, or for

trans-Mediterranean species, the Sahara (see Calosi et al.

2008a). Both summer air maxima and winter minima can

exceed the lethal limits recorded here for Deronectes. For

example, maximum recorded summer temperatures (from

aerial weather stations) along the latitudinal gradient occu-

pied by the species studied range from 34Æ5 �C (Jokkmokk,

Sweden – 66�N; 257 m) to 48Æ1 �C (Marrakech, Morocco –

31�30¢ N; 470 m) (Meteorological Office 1972, 1983). Com-

parably during winter, air temperatures in areas occupied by

these species regularly drop well below their lethal limits,

minimum recorded temperatures ranging from )10Æ8 �C(Bouarfa, Morocco – 32�N; 1310 m) to )43Æ4 �C (Stensele,

Sweden – 65�N; 330 m) (Meteorological Office 1972, 1983).

The direct relevance of extreme air temperatures in the ecol-

ogy of these diving beetles may be limited, however, as these

animals spend almost all of their life histories in a thermally

buffered aquatic medium, only pupation occurring exclu-

sively in air, and this taking place in bankside refugia, which

are themselves thermally buffered (P. Abellan, A. Millan and

D. Sanchez-Fernandez personal communication). Addition-

ally here, whilst our data broadly support Addo-Bediako

et al. (2000) on the extent of variability of UTL and LTLwith

latitude, unusually for temperate insects (see Kingsolver &

Huey 1998; Addo-Bediako et al. 2000; Goto, Kitamura &

Kimura 2000; Klok & Chown 2003; Terblanche et al. 2005)

and other ectotherms (Stillman 2002; Ghalambor et al. 2006;

Deutsch et al. 2008), Deronectes species show only slightly

higher interspecific variability in LTL compared to that

observed for UTL. Again this may result from the fact that

these insects live in a relatively thermally buffered environ-

ment, overwintering in water, where in-stream temperatures

fluctuate 4–5 fold less than those observed in surrounding

air, both daily and seasonally [southern Spain (A. Millan,

P. Abellan andD. Sanchez-Fernandez, personal communica-

tion), North-West Italy (S. Fenoglio and T. Bo, personal

communication) and Australia (B.J. Robson, personal com-

munication)]. In summer, the occurrence of occasional

droughts, and the consequent lack of in-stream thermal pro-

tection, may have selected for heat tolerance, and it is inter-

esting to note that species which live in the most drought-

prone regions are amongst the most tolerant to high tempera-

tures, including D. fairmairei, D. algibensis, D. opatrinus,

D. hispanicus andD.moestusFairmaire.

Conclusions

Given that widespread species of Deronectes are those that

have been most successful in expanding their ranges outside

Pleistocene refugial areas, our results suggest that thermal

Table 2. Model selection to estimate factors influencing southern and northern range boundaries inDeronectes species

Model np AIC DAIC AICweight

Southern limit

UTL + DUTL + DA 4 27Æ636 0Æ000 0Æ532UTL + DUTL + BM + DA 5 29Æ572 1Æ936 0Æ202UTL + DA 3 30Æ460 2Æ824 0Æ130UTL + DUTL 3 31Æ522 3Æ886 0Æ076UTL 2 32Æ016 4Æ380 0Æ060

Southern limit (independent contrasts)

UTL + DUTL + BM + DA 4 )41Æ116 0Æ000 0Æ308UTL + DUTL + BM 3 )41Æ050 0Æ067 0Æ298UTL + DUTL + DA 3 )40Æ676 0Æ440 0Æ247UTL + DUTL 2 )39Æ370 1Æ746 0Æ129UTL + DA 2 )35Æ475 5Æ641 0Æ018

Northern limit

LTL 2 )116Æ930 0Æ000 0Æ405LTL + BM 3 )115Æ609 1Æ3213 0Æ209LTL + DLTL 3 )115Æ012 1Æ9183 0Æ155LTL + DA 3 )114Æ930 2Æ000 0Æ149DA 2 )113Æ753 3Æ177 0Æ083

Northern limit (independent contrasts)

LTL + DLTL + BM 3 )173Æ830 0Æ000 0Æ730LTL + DLTL + BM + DA 4 )171Æ834 1Æ996 0Æ269LTL + DLTL + DA 3 )155Æ147 18Æ684 6Æ41E)05LTL + DLTL 2 )154Æ409 19Æ422 4Æ43E)05LTL 1 )151Æ423 22Æ408 9Æ95E)06

In each case both absolute tolerance and acclimatory ability were included as independent variables (UTL andDUTL or LTL andDLTL respec-

tively), together with bodymass (BM) and dispersal ability (DA) (measured asmeanwing length ⁄ body length ratio). np = number of parame-

ters; AIC = Akaike’s Information Criteria. AICweight represents the likelihood of the model given the data. Parameters with a significant

slope are highlighted in bold.

Species’ geographical range determinants 201

� 2009 TheAuthors. Journal compilation� 2009 British Ecological Society, Journal of Animal Ecology, 79, 194–204

tolerance has influenced post-glacial colonization success.

The genus has its centre of diversity in the Mediterranean

region (Fery & Brancucci 1997; Fery & Hosseinie 1998),

wheremany of the extant species seem to have evolved during

the Pleistocene (Ribera et al. 2001; Ribera & Vogler 2004).

Good post-glacial colonists seems to have been able to retain

southern European populations whilst they expanded north:

the most successful species of all in this regard being D. latus

which has retained populations in the southern Balkans, at

the same time as expanding as far as northern Scandinavia in

the Holocene. Other species may be genuinely restricted by

thermal physiology. Deronectes fairmairei, D. hispanicus and

D. opatrinus, for example, all have relatively high mean

UTLs, and are widespread in the westernMediterranean, but

have poor cold tolerance, and reach their northern range

limits at relatively low latitudes. Deronectes algibensis, the

most narrowly endemic species of the genus in Europe, and

also the one with the most southerly centered range has one

of the highest mean UTLs in the genus, but has the least

developed tolerance of low temperatures. Some other endem-

ics may actually be trapped in southern refugia due to poor

heat tolerance.Deronectes angusi andD. wewalkai, for exam-

ple, are both relatively tolerant of low temperatures, but may

have remained restricted to their southern European moun-

tain ranges by a physiological inability to tolerate heat, and

thus cross intervening lowland areas such as the Ebro valley,

which may form effective barriers to their dispersal (see Ri-

bera 2003). Such species may be particularly at risk in the face

of ongoing and future climate changes, our results suggesting

that restricted endemics tend to be more vulnerable in this

regard than their widespread relatives. Given the added effect

of climatic warming on habitat availability in southern

mountains (Lovejoy & Hannah 2005), these taxa may be

doubly at risk in the future. In contrast, more widespread

species, which are relatively tolerant of high temperatures

(such as D. latus, D. fairmairei, D. moestus, D. opatrinus and

D. hispanicus) may have a better ability to retain their current

geographical ranges in the face of ongoing global climate

change.

Acknowledgements

We thank Pedro Abellan, Mark Briffa, Tiziano Bo, Stefano Feno-

glio, Hans Fery, Andy Foggo, Garth Foster, Andres Millan, Ignacio

Ribera, Brenda Robson, Simon Rundle, David Sanchez-Fernandez,

Jaroslav Stastny, Richard Ticehurst, Ann Torr and Jon Webb for

their assistance, help and support. We thank John S. Terblanche,

Ray B. Huey, and two other anonymous reviewers, for their useful

comments and constructive criticisms. In addition, we are grateful to

Ted Garland for advice on phylogenetic analysis of comparative

data. Finally, we thank Hans Fery, Shidi Hosseinie and Michael

Brancucci for their outstanding systematic work on Deronectes –

without which this study would have been impossible. This investiga-

tion was supported by an award from the Leverhulme Trust to DTB

and JIS.

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Received 28 July 2009; accepted 11May 2009

Handling Editor: Simon Leather

Supporting Information

Additional supporting information may be found in the online ver-

sion of this article.

Appendix S1. Collection localities, southern and northern range lim-

its, latitudinal range extents (LRE) and latitudinal range central

points (LRCP) forDeronectes species studied.

Appendix S2. Body mass, wing size and thermal performance of

Deronectes species.

Please note: As a service to our authors and readers, this journal pro-

vides supporting information supplied by the authors. Suchmaterials

may be re-organized for online delivery, but are not copy-edited or

typeset. Technical support issues arising from supporting informa-

tion (other thanmissing files) should be addressed to the authors.

204 P. Calosi et al.

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