Patterns in body size and melanism along a latitudinal cline in the wingless grasshopper,...

ORIGINALARTICLE

Patterns in body size and melanism alonga latitudinal cline in the winglessgrasshopper, Phaulacridium vittatum

Rebecca Harris1*, Peter McQuillan1 and Lesley Hughes2

1School of Geography and Environmental

Studies, University of Tasmania, Private Bag

78, Hobart 7001, Australia, 2Department of

Biological Sciences, Macquarie University,

North Ryde, NSW, 2109, Australia

*Correspondence: Rebecca Harris, School of

Geography and Environmental Studies,

University of Tasmania, Private Bag 78 Hobart,

7001, Australia.

E-mail: [email protected]

ABSTRACT

Aim We explore geographic variation in body size within the wingless

grasshopper, Phaulacridium vittatum, along a latitudinal gradient, and ask

whether melanism can help explain the existence of clinal variation. We test the

hypotheses that both male and female grasshoppers will be larger and lighter in

colour at lower latitudes, and that reflectance and size will be positively

correlated, as predicted by biophysical theory. We then test the hypothesis that

variability in size and reflectance is thermally driven, by assessing correlations

with temperature and other climatic variables.

Location Sixty-one populations were sampled along the east coast of Australia

between latitudes 27.63� S and 43.10� S, at elevations ranging from 10 to 2000 m

a.s.l.

Methods Average reflectance was used as a measure of melanism and femur

length as an index of body size for 198 adult grasshoppers. Climate variables were

generated by BIOCLIM for each collection locality. Hierarchical partitioning was

used to identify those variables with the most independent influence on

grasshopper size and reflectance.

Results Overall, there was no simple relationship between size and latitude in

P. vittatum. Female body size decreased significantly with latitude, while male

body size was largest at intermediate latitudes. Rainfall was the most important

climatic variable associated with body size of both males and females. Female

body size was also associated with radiation seasonality and male body size with

reflectance. The reflectance of females was not correlated with latitude or body

size, while male reflectance was significantly higher at intermediate latitudes and

positively correlated with body size. Analyses of climate variables showed no

significant association with male reflectance, while female reflectance was

significantly related to the mean temperature of the driest quarter.

Main conclusions Geographic variation in the body size of the wingless

grasshopper is best explained in terms of rainfall and radiation seasonality, rather

than temperature. However, melanism is also a significant influence on body size

in male grasshoppers, suggesting that thermal fitness does play a role in

determining adaptive responses to local conditions in this sex.

Keywords

Acrididae, Australia, Bergmann’s rule, biophysical theory, body size, ectotherm,

geographic variation, Gloger’s rule, latitude, thermal melanism.

Journal of Biogeography (J. Biogeogr.) (2012)

ª 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 1doi:10.1111/j.1365-2699.2012.02710.x

INTRODUCTION

The hypothesis that geographic clines in body size are

temperature driven has attracted research attention for more

than 150 years. Tests of the hypothesis, however, have rarely

considered other morphological characteristics that contribute

to the thermal qualities of an organism, such as colour (Chui &

Doucet, 2009). Here we study interactions between size and

colour at the intraspecific level to investigate how they may

reflect adaptations to local thermal conditions, and therefore

influence the strength of clines in body size.

Temperature has long been considered the main environ-

mental driver of geographic clines in body size. Ectotherms

make up more than 99% of all animal species, and, being

unable to internally regulate their body temperatures, are

directly affected by temperature and climate variables related

to thermoregulation. Insects reared at lower temperatures in

the laboratory take longer to mature and grow to a larger size

(the temperature–size rule) (Ray, 1960; Atkinson, 1994;

Atkinson & Sibly, 1997). It has been estimated that more than

80% of ectotherms follow this pattern, reflecting phenotypic

plasticity to temperature (Atkinson, 1994).

Historically, latitude and elevation have been considered

direct surrogates for temperature, and increases in body size

with latitude and elevation are often referred to as Bergmann’s

rule. Bergmann (1847) proposed that body size of endotherms

decreases with temperature and therefore tends to increase

with colder climates. His explanation was based on a

thermoregulatory mechanism – that larger endotherms have

a thermal advantage in colder environments due to their

smaller surface area-to-volume ratio. Debate has raged ever

since about the applicability of Bergmann’s rule to ectotherms

(Blackburn et al., 1999), whether it should be applied intra- or

interspecifically (James, 1970; Blackburn et al., 1999) and what

mechanism might explain the observed patterns in different

animal groups (Ashton et al., 2000; Watt et al., 2010).

There is an extensive literature describing species that do, or

do not, exhibit clines in body size along latitudinal and

elevational gradients (see reviews by Blackburn et al., 1999;

Meiri & Dayan, 2003; Blanckenhorn & Demont, 2004; Chown

& Gaston, 2010), and different mechanisms have been

proposed to explain observed patterns within and between

species. We concentrate here on explanations for intraspecific

clines in ectotherms (see above reviews for interspecific

hypotheses).

There are two main hypotheses to explain a positive

relationship between size and geographic variables within

species of ectotherms [i.e. larger size at higher latitudes or

elevations (colder environments)]. The first hypothesis is that

high temperatures increase metabolic and maturation rates, in

turn leading to smaller adults (see Chown & Gaston, 2010).

The second hypothesis, known as the starvation resistance

hypothesis, predicts an advantage to larger animals under cold

and more seasonal conditions because of their greater ability to

withstand seasonal declines in food availability (Peters, 1983;

Cushman et al., 1993).

In many insect species, however, intraspecific clines in body

size show the opposite relationship with geographic variables

(Masaki, 1967; Mousseau, 1997; Kubota et al., 2007). For these

cases, which are often referred to as ‘converse Bergmann

clines’, non-temperature driven hypotheses have been devel-

oped. The seasonality hypothesis predicts that body size should

increase with temperature (i.e. be smaller at higher latitudes

and elevations), because season length increases with temper-

ature, allowing longer growth periods. In insect species with

flexible life cycles, this relationship may then reverse at a

transition where the number of generations per growing season

shifts (e.g. from univoltine to bivoltine), and body size then

decreases with latitude, producing a sawtooth body size cline

(Roff, 1980; Johansson, 2003). Under the desiccation resistance

hypothesis, body size is expected to increase with aridity

(James, 1970; Remmert, 1981; Stillwell et al., 2007), because

the reduction in surface area-to-volume ratio in larger animals

increases the ability to withstand desiccation.

A geographic rule that has not received as much attention as

Bergmann’s rule is Bogert’s rule (Gaston et al., 2009); this is

sometimes referred to as the converse of Gloger’s rule

(Rapoport, 1969). This rule refers to clinal variation in colour,

resulting from the thermal benefits of being darker in colder

areas. Intraspecific clines in melanism have been documented

within several insect species along latitudinal (Brakefield,

1984a; Pereboom & Biesmeijer, 2003) and elevational gradients

(Watt, 1968; Berry & Willmer, 1986; Ellers & Boggs, 2002; Karl

et al., 2009), with darker individuals being more prevalent in

colder environments (higher latitudes and elevations). A

thermal explanation is supported by laboratory experiments

that have demonstrated that rearing temperature affects

colour. Individuals of several species have been shown to be

darker when reared at lower temperatures (for example,

butterflies and hoverflies: Marriott & Holloway, 1998).

While geographic variation in melanism and body size has

been studied separately, they have rarely been considered

together, even though many authors invoke a thermal

explanation for the observed patterns (but see Guppy, 1986;

Parkash et al., 2008, 2010). To determine whether intraspecific

body size clines in ectotherms reflect local adaptations to

thermal conditions (Mayr, 1956; Endler, 1977; Gardner et al.,

2009), we need to consider not only body size, but colour as

well, because together they influence the thermal conditions

experienced by an organism.

Biophysical theory tells us that body size will influence the

body temperature of an organism. A small individual will

warm up and cool down more quickly than a larger individual

with exactly the same morphology (Gates, 1980; Monteith &

Unsworth, 1990). However, the colour, or reflectance, of an

organism also has a direct influence on its thermal character-

istics. Darker individuals (lower reflectance) will heat up faster

and reach a higher equilibrium temperature than lighter ones

of the same body size, assuming all else is equal (Gates, 1980;

Monteith & Unsworth, 1990). This has been shown to be the

case under laboratory conditions in beetles (Stewart & Dixon,

1989; de Jong et al., 1996), grasshoppers (Forsman, 1997), bees

R. Harris et al.

2 Journal of Biogeographyª 2012 Blackwell Publishing Ltd

(Pereboom & Biesmeijer, 2003) and butterflies (Watt, 1968,

1969). This biophysical characteristic should provide a thermal

advantage to dark individuals over lighter individuals under

conditions of low ambient temperature. Conversely, lighter

individuals may be at an advantage in hotter conditions, where

dark individuals risk overheating (the thermal melanism

hypothesis) (Clusella-Trullas et al., 2007).

It is possible that in species where geographic clines in

body size are absent or weak, the thermal effects of melanism

are obscuring the relationship between size and temperature.

This would occur if the thermal effects of melanism act in an

opposing direction due to a trade-off between these traits

(assuming an energetic cost is associated with the develop-

ment of melanism). A trade-off between two traits occurs

when an increase in fitness due to a change in one trait is

opposed by a decrease in fitness due to a concomitant change

in the second trait (Roff & Fairbairn, 2007). Because heat

gain is maximized in smaller, darker animals, and minimized

in larger, lighter animals, we would expect a positive

relationship between body size and melanism if there is no

trade-off and the geographic patterns are thermally driven.

An interaction between reflectance and body size would

provide evidence of a trade-off between body size and

melanism. A negative correlation between body size and

melanism could indicate either a direct trade-off, or that

energy is not limiting so that an animal can be, for example,

both large and dark without incurring a fitness cost.

However, for a direct linear trade-off to be detectable, the

cost would need to be equal across all sites and individuals,

with no interaction with any other life-history characteristic

(Roff et al., 2002). As this is highly unlikely, we are more

likely to be able to demonstrate the absence of a trade-off

rather than its presence.

Some authors have suggested that the influence of melanism

on body temperature is too small to have an ecologically

meaningful impact, particularly in small animals (Digby, 1955;

Willmer & Unwin, 1981; Stevenson, 1985; Shine & Kearney,

2001). However, for behavioural thermoregulators that shuttle

between sun and shade to maintain their preferred body

temperature, differences in melanism have been shown to have

a significant impact on body temperature under natural

conditions (Edney, 1971; Clusella-Trullas et al., 2009). Many

grasshopper species, in particular members of the Acrididae,

are strong behavioural thermoregulators (Uvarov, 1966; Wil-

lott, 1997). They utilize solar radiation by basking to maintain

their preferred body temperature, which may differ markedly

from the ambient temperature (Pepper & Hastings, 1952;

Chappell & Whitman, 1990). Grasshopper species that exhibit

clines in body size and colour therefore provide an excellent

opportunity for studying the interaction between body size and

colour.

In this study we explore geographic variation in body size in

the acridid grasshopper, Phaulacridium vittatum (Sjostedt),

along the east coast of Australia (including Tasmania) to

investigate the question: can melanism help explain the

existence of clinal variation in body size within species?

Specifically, we test for correlations between latitude and body

size and/or melanism. On the basis of biophysical theory, we

expect larger grasshoppers to be found at lower (warmer)

latitudes and lower elevations (a converse Bergmann’s cline).

We expect that lighter grasshoppers will also be found at lower

latitudes and lower elevations (Bogert’s rule). Because a

converse Bergmann’s cline could also be generated by season-

ality or desiccation, we test whether clines in body size of P.

vittatum can be explained by variability in temperature or

other climatic variables. We test males and females separately,

because body size and melanism are likely to have different

adaptive consequences in each sex. We expect that body size in

females would be less flexible than in males, given the

fecundity trade-offs this would entail.

MATERIALS AND METHODS

The wingless grasshopper, P. vittatum, is a common species of

Acrididae, widely distributed in open habitats in the cool

temperate areas of eastern and southern Australia (23�36¢ S to

43�06¢ S latitude) (Fig. 1a). It is restricted to higher elevations

in the north, but its elevational range extends from sea level to

1500 m in cooler, more southerly locations, including Tasma-

nia (Key, 1992). Phaulacridium vittatum has an annual life

cycle, overwintering in the egg stage. Hatchlings pass through

five nymphal stages before emerging as adults. The earliest

hatchlings may be observed in the field in late spring, with

adults surviving into late autumn in warmer years (Baker,

2005). Adults can be macropterous, with functional wings, or

brachypterous and incapable of flight (referred to here as

(a)

(b)

Figure 1 (a) The distribution of the wingless grasshopper,

Phaulacridium vittatum, based on museum specimens and (b)

sampling locations along a latitudinal gradient in eastern Australia.

Geographic variation in size and melanism

Journal of Biogeography 3ª 2012 Blackwell Publishing Ltd

‘winged’ and ‘wingless’). These forms occur together in almost

all populations of P. vittatum (Key, 1992). The wingless form is

most abundant in pastures, while in areas dominated by

shrubs, strips along forest margins, and in gardens, the winged

is the more abundant form (Clark, 1967).

Body size is variable in P. vittatum, with females ranging in

length from 12 to 20 mm long and males from 10 to 13 mm

(Baker, 2005). It is polymorphic for colour pattern, with

individuals ranging from light, through to dark brown and

black, and rarely, green. Individuals can be striped, with two

white longitudinal stripes on the dorsal surface, unstriped or

patterned, with very dark lateral surfaces on the pronotum and

a light dorsal surface. All colours are manifested in the winged

and wingless forms, with the exception of the green morph and

the very light patterned form, which are not found in winged

grasshoppers. The range of colour morphs can be present

within the same population, and is set for an individual once it

reaches the adult stage (Key, 1992).

Sampling

Sixty-one populations were sampled between 2006 and 2009

from the east coast of Australia between latitudes 27.63� S and

43.10� S (Fig. 1b). In total, 198 adult grasshoppers (91 females

and 107 males) were collected from roadside verges and open

pastures by hand and with a sweep net. Sample size was not

even across sites, ranging from 1 to 13, with a mean of

3.40 ± 0.35. At the majority of sites (75%), four or fewer

grasshoppers were collected. A hand-held GPS was used to

record the latitude, longitude and elevation of each site.

Elevation ranged from 10 to 2000 m a.s.l. Only unstriped,

wingless adult specimens were considered in the analysis,

because very few striped and winged grasshoppers were

collected and they were not evenly represented along the

latitudinal gradient.

Body size

Body size was estimated using the length of the right femur as a

surrogate, which was measured using handheld vernier calli-

pers (accurate to 0.02 mm). Femur length is closely correlated

with body size and other size metrics in grasshoppers (Masaki,

1967), and is more reliable than body length, which can change

as specimens dry.

The repeatability of the femur measurements was evaluated

by randomly selecting 10 males and 10 females and measuring

each of them 10 times in random order. Repeatability was

calculated as: r ¼ s2A=ðs2 þ s2

AÞ, where s2A is the among-groups

variance component and s2 is the between-groups variance

component, calculated from the mean squares (MS) in the

analysis of variance as s2 = MSw and s2A ¼ ðMSA �MSwÞ=n.

Repeatability falls between 0 and 1 (Lessells & Boag, 1987).

Measurement repeatability was high (males, r = 0.903; F9,90 =

93.85, P < 0.0001; females, r = 0.9305; F9,90 = 136.239,

P < 0.0001).

Reflectance

Reflectance was measured using an Ocean Optics USB2000

spectrophotometer (Ocean Optics Incorporated, Dunedin, FL,

USA) with a PX-2 pulsed xenon light source. Measurements were

taken at an angle of 45�. The spectrophotometer was connected

to a PC running Ocean Optics OOIBase 32 v.1.0.2.0 software

with the integration time set at 7 m/s and each measurement was

averaged 10 times by the software (Bruce et al., 2005). All sample

reflectance spectra were calculated relative to a barium sulphate

white standard, and a dark and white standard reference

spectrum was taken every 10 minutes during measurement of

samples. Measurements were taken in a dark room. The range of

300–700 nm was used, as this was the range of sensitivity of the

machine. Although this range of wavelengths does not encom-

pass the full thermal range of reflectance, we have demonstrated

in laboratory warming experiments that darker individuals

warm more quickly and reach higher equilibrium temperatures

than lighter individuals, and that visual separation of the colour

morphs into distinct categories can be made (see Appendix S1 in

Supporting Information). Ideally, we would have measured

reflectance over the wavelengths 290–2600 nm, to incorporate

the ultraviolet, visible and infra-red parts of the spectrum (Gates,

1980; Nussear et al., 2000; Clusella-Trullas et al., 2007).

However, very few studies have objectively measured reflectance

and our measurements of visible radiation represent a significant

improvement on studies in which the continuum of colour has

been simplified by arbitrarily separating colours into discrete

groups (Roland, 1982).

All specimens were pinned and dried prior to measurement.

Willmer & Unwin (1981) found less than 1% variability when

they compared reflectance of freshly killed and dried insects.

The reflectance was measured at four different positions on

each individual, two on the dorsal surface, one on the side of

the thorax, and one on the lateral surface of the right femur.

The average proportion of light reflected at 5 nm intervals was

calculated for each individual. The mean of these measure-

ments was calculated across all measurements for that

individual to obtain an average.

Climate variables

The BIOCLIM program of the ANUCLIM 5.1 package was

used to estimate 35 climatic variables corresponding to each

collection point along the latitudinal gradient (Houlder et al.,

2000). Principal components analysis (PCA) was used to

explore inter-relationships between environmental variables

and reduce the number of variables needed to adequately

summarize the data (Quinn & Keough, 2002). This was

necessary to reduce the number of variables in the subsequent

hierarchical partitioning analysis, which is limited to testing 12

or fewer independent variables.

Separate PCAs were run on subsets of the climate variables

to choose one representative variable within each of the

categories of temperature, rainfall, radiation and moisture

R. Harris et al.


variables. The variable with the highest loading on each PCA

component 1 was chosen for inclusion in subsequent analyses.

For the temperature subset, the first two components were

required to explain sufficient variability in the data. The

variables chosen and the amount of variability they explained

within each subset were: mean temperature of the driest

quarter (55.7%); temperature seasonality (32.1%); annual

rainfall (91.5%); radiation seasonality (78.1%); and moisture

seasonality (99.9%). The correlation matrix between these

variables and reflectance is shown in Appendix S2.

The choice of these climate variables is justified on the basis

of the known biology and distribution of the wingless

grasshopper. The annual temperature and temperature sea-

sonality can be expected to affect development temperature for

egg and nymphs and the length of the growing season. Annual

rainfall and moisture seasonality will influence the timing of

food availability and quality of food resources, and rainfall is

known to limit the distribution of the wingless grasshopper

towards the inland of mainland Australia. Radiation season-

ality will influence grasshoppers directly, through its effect on

surface temperatures, and indirectly, through its effects on

plant growth and moisture levels.

Statistical methods

Pearson’s correlation coefficient was used to test for associa-

tions between femur length, reflectance, latitude, longitude and

elevation. A randomization test (999 permutations) for the

significance of the correlation coefficient was used because

individual data points from a geographic gradient are not

statistically independent (Cushman et al., 1993; Manly, 1997;

Butler, 2001). Tests were carried out using Minitab version

14.2 (Minitab Inc., 2005) and the CORRELATIONRAN macro

from Butler (2001). All probabilities given refer to those for

two-sided randomizations.

The relationship between variability in size and latitude was

also tested, by calculating the coefficient of variation (CV) of

the mean for males and females in 1� latitudinal bands.

Hierarchical partitioning

Hierarchical partitioning of R2 values was used to identify those

variables with the most independent influence on grasshopper

size and reflectance. This method calculates the proportion of

variance explained independently and jointly by each variable

(Chevan & Sutherland, 1991; Mac Nally, 1996; Walsh & Mac

Nally, 2005), eliminating spurious conclusions based on joint

correlations with other independent variables. Latitude, longi-

tude and elevation were not included, as they are not indepen-

dent of the other variables. Analyses were performed using the R

public-domain statistical package (R Project for Statistical

Computing release 1.9.0, http://www.r-project.org).

Randomization was used to quantify relative ‘effect sizes’

associated with the partitioning, by estimating the z-score

{[observed – mean (randomizations)]/SD(randomizations)}

for each predictor variable, and the statistical significance

based on the upper 95% confidence limit (z ‡ 1.65) (Mac

Nally, 2002; Mac Nally & Walsh, 2004).

RESULTS

Geographic correlates

Body size

With males and females combined, the body size of P. vittatum

was not significantly correlated with latitude (r2 = 0.084,

P = 0.248, n = 198), longitude (r2 = 0.101, P = 0.138,

n = 198) or elevation (r2 = 0.040, P = 1.000, n = 198). How-

ever, female body size showed significant correlations with all

three, being negatively correlated with latitude (r2 = )0.282,

P = 0.006, n = 91), and positively correlated with longitude

(r2 = 0.358, P = 0.002, n = 91) and elevation (r2 = 0.298,

P = 0.010, n = 91). Male body size was not significantly

correlated with elevation (r2 = )0.077, P = 0.452, n = 107) or

longitude (r2 = )0.113, P = 0.250, n = 107) but did show a

quadratic relationship with latitude, being larger at interme-

diate latitudes (Fig. 2a).

Reflectance

Female reflectance was not significantly correlated with any of

the geographic variables (latitude: r2 = 0.052, P = 1.000; longi-

tude: r2 = )0.169, P = 0.108; elevation: r2 = )0.057, P = 1.000)

(Fig. 2b). The average reflectance of males showed a significant

negative correlation with longitude (r2 = )0.230, P = 0.018),

and a significant quadratic relationship with latitude (r2

quadratic = 0.06, P = 0.04) (Fig. 2b). Elevation was not signif-

icantly correlated with reflectance (r2 = 0.018, P = 1.000).

Relationship between body size and reflectance

Average reflectance and body size showed a significant positive

correlation in male, but not in female grasshoppers (males:

r2 = 0.206, P = 0.038; females: r2 = )0.131, P = 0.244)

(Fig. 3). Darker males were smaller than lighter ones.

Variability in body size and reflectance

Phaulacridium vittatum exhibited substantial variability in body

size throughout its range, with femur length of wingless females

(n = 91) ranging from 9.08 to 12.00 mm and that of males

(n = 107) from 6.98 to 9.62 mm. Females, with a mean femur

length of 10.39 ± 0.07 mm, were significantly larger than males,

which had a mean length of 8.25 ± 0.05 mm (F1,196 = 597.16;

P £ 0.0001). Overall, there was a trend towards higher variabil-

ity in body size at higher latitudes, although the relationship was

not significant for females (r2 = 0.327, P = 0.08) or males

separately (r2 = 0.393, P = 0.07) (Fig. 4a).

The average reflectance of P. vittatum ranged from 2.17 to

4.82% in females and from 2.60 to 4.96% in males. Males and

females were significantly different (F1, 196 = 6.74; P = 0.010),



with the mean reflectance of females being 3.64% ± 0.005, and

that of males 3.84% ± 0.004. Variability in reflectance was

unrelated to latitude in female (r2 = 0.025, P = 0.66) or male

grasshoppers (r2 = 0.042, P = 0.59) (Fig. 4b). The area of very

high variation in female reflectance corresponds to an area in

which a wide range of elevations (225–773 m a.s.l.) was

represented.

Climatic correlates

Body size

For female body size, the significant independent correlates

were radiation seasonality (33.0%; z = 5.33) and annual

rainfall (27.4%; z = 4.88). Reflectance was not a significant

contributor to body size, explaining only 2.9% of the

variability (z < 1.65) (Fig. 5a). For male grasshoppers, reflec-

tance and annual rainfall were the only predictor variables to

show a significant effect, each independently explaining a

similar amount of the variability in body size (24.7%, z = 2.26

and 27.4%, z = 1.96, respectively) (Fig. 5b).

In both of these analyses the joint contributions are high

relative to the independent contributions, indicating that the

contribution to shared variability in the full model is high

(Walsh & Mac Nally, 2005). Negative joint contributions

indicate that the majority of the relationships between these

variables and the other predictors are suppressive rather than

additive (Chevan & Sutherland, 1991). In the analysis of female

body size, this is the case for temperature seasonality, while in

males, annual rainfall, moisture seasonality, and to a lesser

extent radiation seasonality, have a negative relationship with

the other variables.

Reflectance

The only predictor variable to show a significant correlation

with the reflectance of female grasshoppers was the mean

temperature of the driest quarter (32.2%, z = 1.75) (Fig. 6a).

Femur length explained the most variability (33.4%) in male

reflectance (Fig. 6b). With a z score of 1.6, it was close to being

significant at the 0.05 level (z = 1.65). None of the other

predictor variables tested were significantly associated with

male reflectance. As with the analyses on body size, the

conjoint contribution of several variables is high, and is

negative in the case of temperature seasonality and annual

rainfall. A summary diagram of significant influences on male

and female body size and reflectance is given in Fig. 7.

Average reflectance0.500.450.400.350.300.250.20

Fem

ur le

ngth

(mm

)

12.0

11.0

10.0

9.0

8.0

7.0

Figure 3 Relationship between body size and average reflectance

in females (n = 91) (closed circles, unbroken line) and males

(n = 107) (open circles, dashed line) of the wingless grasshopper,

Phaulacridium vittatum. The fit is significant for males (male

femur length = 7.28 + 2.54 · reflectance) but not females.

Figure 2 (a) Femur length and (b) average reflectance of females

(n = 91) (closed circles) and males (n = 107) (open circles) of the

wingless grasshopper, Phaulacridium vittatum, along a latitudinal

gradient in eastern Australia. The fit for femur length is significant

for females (unbroken line) (femur length = 11.661827 ) 0.0354277

· latitude) and males (dashed line) [femur length = 8.1 + 0.008 ·latitude ) 0.007(latitude ) 35.71)2]. The fit for average reflectance

is significant for males (dashed line) [reflectance = 0.32

+ 0.002 · latitude ) 0.0004 · (latitude ) 35.7069)2], but not

females (unbroken line).

R. Harris et al.


DISCUSSION

Overall, there was no significant relationship between body size

and latitude in P. vittatum, but by considering the sexes

separately and including the influence of melanism we revealed

a number of significant, and contrasting, patterns. Female

body size decreased with latitude, while males were largest at

intermediate latitudes. Female body size responded to changes

in local conditions and was unrelated to average reflectance,

while for males variability in body size appeared to be

compensated for by associated changes in melanism.

Female body size

The negative correlation demonstrated at the broad scale

between female body size and latitude is similar to that found

in other studies of grasshoppers, with larger grasshoppers

being found at lower latitudes (Masaki, 1967; Mousseau &

Roff, 1989; Telfer & Hassall, 1999; Bidau & Martı, 2007a, b; Ho

et al., 2010). This relationship has generally been attributed to

differences in season length and development time. Our data

support this conclusion, but also suggest that rainfall is an

important influence, interacting with radiation seasonality to

generate the observed geographic variability.

The analysis of climate variables along the latitudinal

gradient showed that, for females, the most influential climate

variables were related to radiation seasonality and annual

rainfall, not to temperature. In univoltine species such as

P. vittatum which have a long development time relative to the

length of the growing season, a shorter growing season will

limit the time available for feeding, growth and development

and therefore the body size that can be attained (Mousseau,

1997; Blanckenhorn & Demont, 2004). Field observations

suggest that grasshoppers quickly become inactive in cloudy

conditions, so environments that are more seasonal in terms

Figure 4 Relationship between latitude and coefficient of varia-

tion of (a) femur length and (b) average reflectance in females

(n = 91) (r2 = 0.327, P = 0.08) (closed circles) and males

(n = 107) (r2 = 0.393, P = 0.07) (open circles) of the wingless

grasshopper, Phaulacridium vittatum. Latitude is in one degree

bands.

-120

-100

-80

-60

-40

-20

0

20

40

60

80

100

120

Reflectance Temperatureseasonality

Meantemperaturedriest quarter

AnnualRainfall

Radiationseasonality

Moistureseasonality

Expl

aine

d va

rianc

e (%

)

(a)

-120

-100

-80

-60

-40

-20

0

20

40

60

80

100

120

Reflectance Temperatureseasonality


AnnualRainfall


Moistureseasonality

Expl

aine

d va

rianc

e (%

)

(b)

* *

* *

Figure 5 Percentage of variance in the body size of (a) females

(n = 91) and (b) males (n = 107) of the wingless grasshopper,

Phaulacridium vittatum, explained independently (open bars) and

jointly (striped bars) by six predictor variables. Significant inde-

pendent correlates are indicated by an asterisk.



of sunlight represent a shorter available growing season.

Additionally, in more seasonal environments, which are also

more changeable on short time scales, smaller grasshoppers

would benefit from more rapid warming when basking to

maintain their preferred body temperature. The importance of

rainfall is likely to reflect the presence of clouds, but may also

indicate the importance of moisture, which has been suggested

to be a better predictor of insect body size than temperature

because the lower surface-area-to volume ratio of larger insects

reduces the risk of desiccation (Remmert, 1981; Stillwell et al.,

2007; Parkash et al., 2009).

Male body size

Male grasshoppers exhibited a quadratic relationship between

latitude and body size, with a higher representation of larger

males at intermediate latitudes. This pattern has been

explained in terms of resource availability in mammals (Geist,

1987), but the decline in body size occurs at very high

latitudes. Here we find that male grasshoppers also tend to be

lighter at intermediate latitudes, suggesting that thermoregu-

latory fitness is a factor in the relationship between body size

and melanism.

As with females, annual rainfall was identified as an important

climatic factor associated with male body size. However,

reflectance also explained almost 25% of the variability in body

size. In contrast with females, no seasonality variable explained a

significant amount of variability in male body size. Season length

affects fitness through trade-offs between the advantages of

being large and the risks associated with the extra development

time required to reach a larger size (Mousseau & Roff, 1989). For

females, the benefits of increased fecundity with greater size may

outweigh the risks (Walters & Hassall, 2006), but males may

benefit more by emerging earlier in the season to increase the

chances of paternity (Zonneveld, 1996).

We speculate that increased melanism in males then

compensates for the thermal consequences of being small. It

is possible that a trade-off occurs between fecundity and

thermoregulation in females, reducing the strength of the

direct relationship between melanism and body size. In males,

on the other hand, which are under selection pressure

-120

-100

-80

-60

-40

-20

0

20

40

60

80

100

120

Femur length Temperatureseasonality


AnnualRainfall


Moistureseasonality

Expl

aine

d va

rianc

e (%

)(a)

-120

-100

-80

-60

-40

-20

0

20

40

60

80

100

120

Femur length Temperatureseasonality


AnnualRainfall


Moistureseasonality

Expl

aine

d va

rianc

e (%

)

(b)

*

(*)

Figure 6 Percentage of variance in the reflectance of (a) females

(n = 91) and (b) males (n = 107) of the wingless grasshopper,

Phaulacridium vittatum, explained independently (open bars) and

jointly (striped bars) by six predictor variables. Significant inde-

pendent correlates are indicated by an asterisk.

Reflectance

+

Body Size

x2

-

--+

Longitude

Latitude

Reflectance24.7%

Longitude

Latitude

Altitude

Annual Rainfall27.4%

Annual Rainfall27.4%

Radiation Seasonality

33.0%

Mean temperature of the driest

quarter 32.2%

Femur length 33.4%

Figure 7 Summary of significant influences on body size and

reflectance in the wingless grasshopper, Phaulacridium vittatum,

along a latitudinal cline on the east coast of Australia. The size of

the circle reflects the relative importance of the variable as deter-

mined by the percentage independent contribution from the

hierarchical partitioning analysis. The direction of the correlation

is indicated where significant linear correlations were found. Black

arrows indicate significant variables and correlations; the open

arrow indicates a non-significant correlation. Bold circles repre-

sent morphological characteristics and plain circles represent cli-

mate variables.

R. Harris et al.


favouring smaller body size, the interaction between melanism

and body size plays an important role in maintaining

geographic variation in body size.

The inter-relationship between body size and reflectance in

males suggests that these morphological characteristics and

thermoregulatory behaviour are co-adapted (Clusella-Trullas

et al., 2007). In laboratory experiments with P. vittatum, darker

grasshoppers select higher preferred temperatures in a thermal

gradient, and when colour is manipulated experimentally, the

preferred temperature chosen changes to reflect the new colour

(R. Harris, unpublished data). Behavioural thermoregulation

therefore shifts to parallel the thermal capacity of the new colour.

Forsman (2000) similarly linked colour and thermoregulation in

grasshoppers, with dark morphs preferring higher body temper-

atures than light morphs. Further research using common garden

experiments or reciprocal transplant experiments would enable

us to determine how much of the geographic variation in size or

colour is due to genetic differences, and how much is due to

phenotypic plasticity of individuals developing under different

conditions (Conover & Schultz, 1995; Arnett & Gotelli, 1999a;

Alho et al., 2010; Stillwell, 2010).

Detecting a trade-off between size and melanism is likely to

be confounded by a range of ecological and evolutionary

factors. For example, it is possible that an increase in size may

be the result of increased fitness in melanistic individuals

(Clusella-Trullas et al., 2007). Trade-offs could occur in

different directions in different populations or habitats,

depending on a range of factors such as variation in the

thermal qualities of a site, food quality, water availability and

competition (McNab, 1971; Chown & Gaston, 2010; Ho et al.,

2010). Characteristics of populations such as density and

habitat patchiness would also affect gene flow and the potential

for local adaptation (Arnett & Gotelli, 1999b). These factors

explain why the wingless grasshopper exhibits moderate

variability in size at all localities throughout its range. With

so much potential for complex inter-relationships, correlative

approaches are unlikely to demonstrate strong relationships

between size and melanism. To disentangle the relationship

between size and reflectance would require experiments to test

specific hypotheses regarding particular characteristics.

Relationship between reflectance, body size

and climate

One of the primary predictions of the thermal melanism

hypothesis is that reflectance should be positively correlated

with solar radiation and/or temperature (Clusella-Trullas et al.,

2008). This was the case for female, but not male, grasshoppers

in this study. The mean temperature of the driest quarter was a

significant influence on female reflectance, but there were no

significant climatic correlates with male reflectance. However,

the majority of the variability in male reflectance was explained

by body size (marginally significant), which from a biophysical

viewpoint also supports a thermal explanation.

The reflectance of male grasshoppers was also significantly

correlated with longitude, with darker males predominating

towards coastal areas. This once again conforms to a thermal

explanation because coastal areas have a cooler and more

stable thermal regime, with less extreme temperatures and

lower variability than areas further inland. This relationship

has been demonstrated in reptiles, with darker reptiles being

found more in coastal and peninsular areas (Clusella-Trullas

et al., 2007).

In addition to thermal melanism, there are several adaptive

reasons for melanism in insects. These include camouflage and

crypsis, which can improve predation avoidance and prey

capture, warning coloration, UV screening and mate attraction

(Majerus, 1998). Some melanisms may also be by-products of

other biochemical systems, such as parasite resistance (Karl

et al., 2010), or occur by chance (Majerus, 1998). In many cases,

when the thermal importance of melanism has been studied,

several factors, such as mimicry, sexual selection and thermal

selective pressures have been shown to play a role (Brakefield,

1984b, 1985). Of the very few studies that have considered

geographic variation in body size and melanism together,

Guppy (1986) demonstrated that temperature alone could not

account for variation in butterfly body size, and that melaniza-

tion of the different areas of butterfly wings was the result of

different adaptive pressures. Melanism of the basal area of the

hind wings was related to different thermal regimes at different

elevations, but melanism of the forewings was determined by

other factors such as predation. Complex interactions such as

these are likely to exist within populations of the wingless

grasshopper, particularly in light of its polymorphism with

respect to the presence of stripes and wings. Although these

morphs were not considered in the present study because of

their low representation in natural populations [for example,

only 5% of winged individuals in pasture populations (Key,

1992)], improved predator avoidance by striped individuals or

greater dispersal in winged individuals may represent different

trade-offs with thermal characteristics.

The patterns shown here suggest that variation in body size

and melanism is advantageous and has developed in response

to local conditions. With quantitative data on fitness, such as

improvements to growth, fecundity or survival, providing the

link from phenotype to improved performance and fitness

(Koehl, 1996; Kingsolver & Huey, 1998; Bidau & Martı,

2007a), this adaptive explanation for variability in body size or

melanism in P. vittatum could readily be tested.

CONCLUSIONS

Selection for body size is mediated by different factors in males

and females of the wingless grasshopper. Female body size is

associated with annual rainfall and radiation seasonality, as is

common in insects that exhibit a negative relationship between

body size and latitude. In male grasshoppers, in which basking

plays an important thermoregulatory role, geographic patterns

in body size are also strongly influenced by reflectance. The

thermal effects of melanism could explain why many investi-

gations have failed to demonstrate strong or consistent

geographic clines in insect body size.



ACKNOWLEDGEMENTS

We thank Mariella Herberstein (Macquarie University) for the

use of the spectrometer. R.M.H. was the recipient of an

Australian Postgraduate Award, and the study was partially

funded by an ANZ (Australia and New Zealand Banking

Group) Holsworth Wildlife Research Endowment.

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the

online version of this article:

Appendix S1 Thermal properties of colour morphs of

Phaulacridium vittatum.

Appendix S2 Correlation matrix of variables selected from

principal components analyses and used in the final hierar-

chical partitioning analyses.

As a service to our authors and readers, this journal provides

supporting information supplied by the authors. Such mate-

rials are peer-reviewed and may be re-organized for online

delivery, but are not copy-edited or typeset. Technical support

issues arising from supporting information (other than

missing files) should be addressed to the authors.

BIOSKETCHES

Rebecca Harris’ research covers the thermal biology and

biophysical and behavioural ecology of insects. Her interests

lie in the conservation of biodiversity and adaptation to

climate change.

Peter McQuillan teaches biogeography and conducts

research into the distribution and conservation of inverte-

brates. He has a special interest in insect–plant–environment

associations in the montane habitats and temperate rainforests

in Tasmania.

Lesley Hughes is an ecologist whose main research interests

are the potential impacts of climate change on Australian

species and ecosystems, conservation policy, and the evolution

of insect–plant interactions.

Editor: Melodie McGeoch

R. Harris et al.


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