Interpopulation variation in sexual dichromatism in the Neotropical grasshopper Sphenarium purpurascens (Orthoptera: Pyrgomorphidae)
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Biological Journal of the Linnean Society, 2021, 132, 900–911. With 4 figures.
Interpopulation variation in sexual dichromatism in
the Neotropical grasshopper Sphenarium purpurascens
(Orthoptera: Pyrgomorphidae)
RAÚL CUEVA DEL CASTILLO*, , MIGUEL GONZÁLEZ-ZERTUCHE and
VÍCTOR HUGO RAMÍREZ-DELGADO
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UBIPRO, Laboratorio de Ecología, FES Iztacala, Universidad Nacional Autónoma de México, A.P. 314,
Tlalnepantla, Estatado de México, CP 54090, Mexico
Received 6 October 2020; revised 15 December 2020; accepted for publication 16 December 2020
Cryptic coloration is an adaptative defensive mechanism against predators. Colour patterns appear cryptic through
general background coloration matching or disruptive coloration. Disruptive coloration might evolve in visually
heterogeneous microhabitats, whereas background matching could be favoured in chromatically homogeneous
microhabitats. In this study, we used digital photography to explore the potential use of disruptive coloration and
background matching in males and females of the Neotropical grasshopper Sphenarium purpurascens in different
habitats. We found chromatic differences in three habitats and sexual dichromatism that might be explained by local
adaptation. Although females and males were sexually dichromatic, interpopulation differences were found in the
magnitude of the sexual dichromatism. In a highly contrasting environment, both males and females seemed to follow
a disruptive strategy, whereas in a heterogeneous environments males and females followed different colour cryptic
strategies, in which males were more disruptive than females, and females exhibited high background matching with
fewer disruptive elements. Selective predation in different microhabitats and differences in mobility between the
sexes might explain the colour pattern divergence between females and males.
ADDITIONAL KEYWORDS: background matching – crypsis – disruptive coloration – photographic analysis –
sexual dichromatism – Sphenarium purpurascens.
INTRODUCTION because it breaks the outlines of the organisms
independently of the variable background patterns,
Cryptic coloration is an adaptative defensive
and it can be adaptative in organisms with high
mechanism against predators and is probably the
mobility (Stevens et al., 2006a, b). Given that crypsis
most widespread form of concealment (Merilaita &
decreases the probability of detection by predators, its
Lind, 2005; Merilaita et al., 2017). Colour patterns
variation usually matches the geographical variation
appear cryptic by background matching (colours that
in substrate colour (Endler, 1990; Stuart-Fox & Ord,
resemble the general colour of the visual background)
2004; Rosenblum, 2006; Marshall et al., 2015; Hantak
or disruptive coloration (patterns that conceal the
& Kuchta, 2018). Moreover, if females and males use
body outline of an animal; Norris & Lowe, 1964).
different microhabitats owing to their different sexual
Background matching can be favoured in chromatically
roles, natural selection towards crypsis can favour a
homogeneous microhabitats (Robledo-Ospina et al.,
divergence in cryptic colour patterns between females
2017; Orton & McBrayer, 2019), but it can be ineffective
and males (Forsman & Appelqvist, 1999; Medina et al.,
at reducing the risk of detection when animals are
2016; Ramírez-Delgado & Cueva del Castillo, 2020).
in motion in heterogeneous environments (Ioannou
& Krause 2009). In contrast, disruptive coloration Sexual dichromatism is understudied. Studies have
could evolve in visually heterogeneous microhabitats focused mainly on vertebrates (Font et al., 2009),
and it has been explained by differences in selective
pressures imposed by visual predators in only a few
*Correponding author. E-mail: rcueva@ecologia.unam.mx cases (Orton & McBrayer, 2019). Examples of crypsis
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911 900SEXUAL DICHROMATISM IN A GRASSHOPPER 901
mediating the differences in coloration between environmental heterogeneity. In the areas surrounding
females and males are found in many bird species, Mexico City, nymphs emerge mainly at the beginning
although in these cases the females tend to be cryptic of the rainy season (early June). Adults mostly appear
because of predation pressures, whereas males are and reproduce during autumn (mid-August to mid-
conspicuous owing to sexual selection (Badyaev & December). Oviposition and death occur at the end of
Hill, 2003; Medina et al., 2017). In invertebrates, autumn and beginning of winter, approximately from
the study of the evolution of sexual dimorphism in mid-October to mid-December (Cueva del Castillo
colour patterns has focused on arthropods and is et al., 1999). However, at low elevations, its life cycle can
poorly documented (Forsman & Appelqvist, 1999; Li start at the beginning of May and end late in January
et al., 2008; Ramírez-Delgado & Cueva del Castillo, (R. Cueva del Castillo, pers. obs.). Thus, temperate and
2020). Given that many cryptic species are sexually dry forests, rain forests and even deserts are found
dichromatic, their study has profound implications in the distribution range of S. purpurascens, only
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regarding the evolution of intraspecific chromatic a short distance away from each other at the same
variation with respect to selective pressures imposed latitude (Sanabria-Urbán & Cueva del Castillo, 2020),
by visual predators. providing the opportunity to explore local chromatic
Cryptic coloration is common in grasshoppers adaptation to diverse environments in this species.
(Eterovick et al., 1997; Forsman & Appelqvist, 1999; Sphenarium purpurascens, like most species in
Ahnesjö & Forsman, 2006; Karpestam et al., 2012; the genus, exhibits wide colour variation (Sanabria-
Baños-Villalba et al., 2018; Edelaar et al., 2019), and Urbán et al., 2017), which suggests substantial
yet the evolution of sexual dimorphism in colour genetic and/or plastic variation and low phylogenetic
patterns in this group of insects has been poorly constraints on its chromatic evolution (Blomberg &
documented (Ramírez-Delgado & Cueva del Castillo, Garland 2002). The dorsal colours of S. purpurascens
2020). Sphenarium purpurascens is an univoltine vary from green to shades of brown or grey (Fig. 1).
generalist herbivore; adults are found in herbs, grass Males and females have longitudinal and transverse
and bush leaves. The species has a broad distribution bands over the thorax and abdomen, showing
and elevation range in central Mexico, from 800 to extensive continuous variation. However, males
2700 m a.s.l., from the southern Altiplano to the Sierra usually exhibit considerably more variation in the
Madre del Sur in the Mexican states of Guanajuato, patterns and number of bands than females, which
Hidalgo, Mexico, Mexico City, Michoacán, Oaxaca, tend to have areas that are coloured more evenly
Puebla, Queretaro, Tlaxcala and Veracruz. The (Sanabria-Urbán et al., 2017). Males and females
western and eastern mountain ranges create high mate randomly with respect to male and female
Figure 1. Dorsal views of the grasshoppers. A, B, female (A) and male (B) from Morelia. C, D, female (C) and male (D)
from Pedregal. E, F, female (E) and male (F) from Tlaxcala. G, dorsal view of female, indicating the dorsal surface of the
grasshopper (GDS) and the adjacent background surface (BS).
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911902 R. CUEVA DEL CASTILLO ET AL.
colour patterns (Cueva del Castillo & Cano-Santana, established. It was then collected by hand, placed in a
2001). Females are less mobile than males and can plastic bag (15 cm × 10 cm) and put into a cooler until it
be found near the ground, where they lay their eggs was unable to move. Each grasshopper was returned to
(Camacho Castillo, 1999). In contrast, males are the same spot where it was first seen (usually on leaves
often found on top of plants, where they actively look or plant stems), and photographs of both the dorsal
for females (R. Cueva del Castillo, pers. obs.). They view of the grasshopper and the background where
are predated by many vertebrates, including birds, it was placed were taken (Fig. 1G). After taken the
mammals and reptiles (Kevan, 1977). photographs, the grasshoppers were placed temporarily
Owing to the environmental complexity of the in a plastic bag in order to avoid their potential
distribution range of S. purpurascens and the broad recapture. Grasshoppers that moved or fled in response
variety of potential visual predators of this species, we to the approaching collectors were discarded from the
expected to find differences in the chromatic patterns study. In all cases, photographs were taken with a
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of the three analysed populations and that the patterns Nikon D3200 camera fitted with an AF-S NIKKOR
of grasshoppers associated with places having higher 18–55 mm, f/3.5–5.6 lens. Camera modifications to
visual complexity would be more diverse. In addition, allow sensitivity to the ultraviolet spectrum were not
given that males and females behave differently and can implemented; therefore, our analysis is restricted to
be found in niches with different chromatic composition, the visible spectrum. However, previous studies have
we expected to find differences in their cryptic strategies. shown marginal reflectance of ultraviolet light on
grasshoppers (Tsurui et al., 2010). All photographs were
taken in field conditions between 11.00 and 14.00 h in
broad daylight. A white diffuser umbrella was placed
MATERIAL AND METHODS over each grasshopper in order to remove potential
shadows. All photographs were taken 40–50 cm away
Study sites and image acquisition from the grasshopper and included a ColorChecker card
We took photographs of male and female grasshoppers (X-rite ColorChecker Passport Photo 2; Munsell Color
from three populations located in Mexico City, specifically Laboratories) in the same plane as the grasshopper and
in Pedregal de San Ángel (19°19′07.9ʺN, 99°11′33.7ʺW), its background. After the photographs were taken, all
and in the outskirts of the cities of Tlaxcala (19°23′17.0ʺN, grasshoppers were released at the same places where
98°12′49.4ʺW) and Morelia (819°70′44ʺN, 101°11′94ʺW). they were collected. Following the suggestions of Stevens
Images of adult grasshoppers and their backgrounds et al. (2007) and Troscianko & Stevens (2015) on taking
were acquired in the middle of the rainy season, during objective measurements from digital photographs, we
the first and second weeks of October 2018, when took the photographs as follows: focal distance was
most of the individuals in the populations were adults constant at 55 mm; aperture was set to f-stop: f/5.6; light
and the vegetation was still green. Pedregal de San sensitivity value (ISO) was set to 400 in all photographs;
Ángel was chosen because of its high environmental and the shutter speed was adjusted in every shot to
heterogeneity (see Ramírez-Delgado & Cueva del prevent overexposure of the pictures. Images were
Castillo, 2020). In contrast, the Tlaxcala location was stored as RAW images to avoid information loss.
at the border of an oak–pine forest, and the Morelia site
was a grassland, dominated mainly by one grass species.
Given their plant diversity, Pedregal de San Angel and Image analyses
Morelia represent the most complex and the simplest Using the multispectral image calibration and analysis
environments, respectively. These localities allowed us (MICA) toolbox v.2.0 (Troscianko & Stevens, 2015)
to test the potentially different cryptic strategies in for I mage J v.1.52 (Schneider et al., 2012) software
males and females of S. purpurascens (Fig. 1) associated and making use of the ColorChecker included in the
with three contrasting environments. photographs, we converted the images into human
At each of the three collection sites, three people cone-catch images. This conversion produces images
walked slowly over the area, searching for grasshoppers. based on the spectral sensitivities of the human visual
Humans can be considered as regular predators of system (Osorio & Vorobyev, 2005, 2008; Delhey et al.,
S. purpurascens because they have collected and 2015).
used these grasshoppers as a food resource since
pre-Columbian times (Sanabria-Urbán & Cueva
del Castillo, 2020). Moreover, in certain conditions, Background matching
humans and birds perform similarly in detection tasks We measured the background matching of the
(Dukas & Kamil, 2001; Michalis et al., 2017). colour and brightness of the morphs against their
Particular care was taken not to disturb any detected background using chromatic and achromatic just
grasshoppers. When one was found, its location was noticeable differences (JNDs) from the cone-catch
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911SEXUAL DICHROMATISM IN A GRASSHOPPER 903
images. Low JND values denote high resemblance superior to other pattern metrics algorithms tested in
between surfaces, whereas high JND values denote humans (see Troscianko et al., 2017). The GabRat tool
low resemblance between two surfaces (Osorio & is based on a Gabor band-pass filter (see Troscianko
Vorobyev, 2008; Troscianko & Stevens, 2015). et al., 2017; Price et al., 2019). Before using this tool,
we converted the cone-catch images into LAB images.
LAB images fit roughly with human luminance and
Pattern analysis colour perception and allow us to measure chromatic
We performed a granularity analysis based on fast disruption (Troscianko et al., 2017). These images
Fourier band-pass filtering from the cone-catch images are composed of three channels: L corresponds to
to evaluate the colour patterns. Band-pass filters allow an achromatic channel (lightness), and A and B to
information at different spatial scales to be separated chromatic channels (red to yellow and blue to green,
(for details, see Chiao et al., 2009; Stoddard & Stevens, respectively) (Kim et al., 2000). The GabRat tool
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2010). Granularity analysis measures the standard estimates the coherent and false edges of an object in an
deviation of pixel reflectance at different pixel scales, image. The analysis produces values ranging from zero
known as filter sizes; this measurement is referred to one, where values close to zero are non-disruptive.
to as energy. The graphical representation of energy
across the different filter sizes generates an energy
spectrum, which is useful to compare energy patterns Statistical analyses
between surfaces (Chiao et al., 2009). This analysis Background colour matching
bears a loose resemblance to the cognitive processing To explore the chromatic and achromatic JNDs,
of visual information by an animal, with decomposition we performed a multivariate analysis of variance
of spatial information into different spatial frequencies (MANOVA) considering locality, sex and locality × sex
(Godfrey et al., 1987; Stevens, 2011; Stoddard & interaction. Data were transformed by quadratic
Osorio, 2019). Granularity analysis has been used to square to meet the test assumptions. Given that
distinguish matches in background patterns (Chiao the MANOVA was significant (see results below),
et al., 2009; Tyrie et al., 2015) and to mark contrasts, additional univariate analyses of variance (ANOVAs)
which are typically found in disruptive colour patterns were performed to detect the significant parameters of
(Robledo-Ospina et al., 2017). Granularity analysis the analysis.
has been used to measure the pattern markings of
several species of animals, including zebras and lions
(Godfrey et al., 1987), cuttlefish (Barbosa et al., 2008; Comparisons of grasshopper dorsal surface
Chiao et al., 2009), fish (Tyrie et al., 2015), spiders pattern between localities and sexes
(Robledo-Ospina et al., 2017) and eggs (Stoddard & A MANOVA considering locality, sex and locality × sex
Stevens, 2010; Yang et al., 2015), in addition to other interaction was performed to explore potential
Sphenarium grasshoppers (Ramírez-Delgado & Cueva differences between the parameters (size of dominant
del Castillo, 2020). marking, pattern diversity and overall pattern
We used the average pixel reflectance of red and contrast of the grasshopper dorsal surface). Before
green channels to calculate the energy spectrum of running the analysis, the data were ln-transformed
grasshoppers and their background across 15 filters to meet the test assumptions. Additional ANOVAs
ranging from two to 256 pixels, in increments of and Tukey’s honestly significant difference (HSD) test
multiples of √2. We obtained three descriptive variables were performed to identify the significant parameters
from the energy spectrum: the filter size at which the of the analysis.
maximum energy peak of the spectrum is reached (size
of dominant marking); the proportion of the energy
peak of the spectrum compared with the rest of the Comparisons of background surface pattern
spectrum (pattern diversity); and the total energy of between localities and sexes
the spectrum (overall contrast between patterns). A MANOVA considering locality, sex and locality × sex
interaction was performed to explore potential
differences between the parameters (size of dominant
Disruptive coloration marking, pattern diversity and overall pattern contrast
We evaluated the edge disruption of the grasshoppers against the surfaces of the backgrounds where the
using the GabRat tool implemented in the MICA grasshoppers were found). Before analysis, the data
toolbox. We used the GabRat tool to measure the ratio were ln-transformed to meet the test assumptions.
between false and coherent edges of the surfaces of the Additional ANOVAs and Tukey’s HSD tests were
grasshoppers. This metric is one of the best predictors performed to detect the significant parameters of the
of human detection time of disruptive targets, and it is analysis.
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911904 R. CUEVA DEL CASTILLO ET AL.
Comparison between dorsal grasshopper surface were not significant, they were not included in the
and background for females and males univariate models.
In order to compare the grasshoppers from the three The ANOVA for the chromatic JND detected
localities with their backgrounds, we performed significant differences between females and males.
Student’s paired t tests comparing the dorsal surfaces The background colour matching was higher (lower
(size of dominant markings and pattern diversity) of values) in females than in males (Table 1A; Fig. 2A).
the grasshoppers with the background surfaces where Also, the ANOVA for the achromatic JND indicated
they were placed. that the differences between the sexes were highly
significant (Table 1B). The achromatic background
matching in male grasshoppers was lower (higher
Disruptive coloration JND) than in females, indicating a low resemblance to
We performed a MANOVA considering locality, sex the background (Fig. 2B).
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and locality × sex interaction to explore the GabRat
in the different channels of the LAB images. The data
were ln-transformed to meet the test assumptions. Comparisons of grasshopper dorsal surfaces
Given that the MANOVA was significant (see results), between localities and sexes
additional ANOVAs and Tukey’s HSD tests were The MANOVA indicated differences between the three
performed to detect the significant parameters of the localities and between male and female dorsal surfaces
analysis. Statistical analyses were performed with R (locality: Wilks’s λ = 0.69, F6,294 = 10.18, P < 0.0001; sex:
v.4.0 (R Core Team, 2020). Wilks’s λ = 0.39, F3,147 = 75.21, P < 0.0001). Nevertheless,
the magnitude of the differences between males and
females in the three localities was similar (locality × sex:
λ = 0.93, F6,294 = 1.79, P = 0.10). Given that the locality × sex
RESULTS
interaction was not significant, it was not included in
We obtained 155 photographs of the dorsal areas the univariate models. There were differences in the
and backgrounds of S. purpurascens from the three size of dominant markings of grasshoppers between the
localities. Twenty-six photographs of females and 31 localities and between females and males.
of males were taken in Pedregal de San Ángel, 26 of The grasshoppers from Morelia had slightly larger
females and 32 of males in Tlaxcala, and 20 of females dominant marks than those from the other localities.
and 20 of males in Morelia. Moreover, females had larger dominant marks than
males (Table 2A; Fig. 3A). Regarding the diversity
of dorsal patterns, the grasshoppers from Morelia
Background colour matching and their backgrounds exhibited greater pattern
The MANOVA indicated significant differences only diversity (i.e. pattern heterogeneity). Only males
for sex in chromatic and achromatic JNDs. There were from Tlaxcala had significantly more patterns than
no differences between localities or population × sex females in their locality (Table 2B, 2E; Fig. 3B). The
interactions (locality: Wilks’s λ = 0.97, F4,296 = 0.82, contrast of the overall patterns of the dorsal surfaces
P = 0.52; sex: Wilks’s λ = 0.84, F2,148 = 14.56, P < 0.0001; of grasshoppers showed highly significant differences
locality × sex: Wilks’s λ = 0.95, F4,296 = 1.92, P = 0.11). between the three localities and the sexes. The
Thus, background colour matching and resemblance to grasshoppers from Morelia had more contrasting
the background were similar in the three populations. patterns than those from the other localities.
Given that locality and locality × sex interaction Moreover, patterns of males contrasted more than
Table 1. ANOVAs of the chromatic (A) and achromatic (B) just noticeable differences (JNDs) between the dorsal surface
of the grasshoppers and their background
Source d.f. Sum of squares Mean square F-value P-value
(A) Chromatic JND
Sex 1 1.171 1.17 8.26 0.0046
Residuals 153 21.61 0.14
(B) Achromatic JND
Sex 1 13.52 13.52 25.35 < 0.0001
Residuals 153 81.61 0.53
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911SEXUAL DICHROMATISM IN A GRASSHOPPER 905
Comparison between grasshopper dorsal
surface and background for females and males
When we compared female and male dorsal chromatic
patterns with their respective backgrounds for the
three sampled localities, we found that both the size
of the dominant markings and the pattern diversity
of the dorsal surface of females matched their
background (Table 3A, 3C, 3D), whereas their overall
pattern contrast differed from their background. In
contrast, the males from the three populations showed
significant differences between their dominant
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markings and the overall contrast of their background
(Table 3B, 3D, 3F). Only males from Tlaxcala showed
significant differences between pattern diversity and
background diversity (Table 3F).
Disruptive coloration (GabRat) of the
grasshoppers from different localities
The MANOVA indicated significant differences for the
disruptive coloration between locality, sex and their
interaction (locality: Wilks’s λ = 0.62, F6,294 = 13.20,
P < 0.0001; sex: Wilks’s λ = 0.74, F3,147 = 17.08, P < 0.0001;
locality × sex: Wilks’s λ = 0.86, F6,294 = 3.94, P = 0.0008).
The GabRat values of the three grasshopper localities
were relatively low (maximum GabRat values: L = 0.37,
A = 0.51 and B = 0.46; minimum GabRat values:
L = 0.5, A = 0.10 and B = 0.07; and mean GabRat
values: L = 0.10, A = 0.21 and B = 0.14), suggesting
a relatively low disruptivity (Troscianko et al., 2018).
Nevertheless, we found significant differences between
localities. The GabRat for the L channel (achromatic
channel) showed significant differences between the
localities; grasshoppers from Morelia had the highest
disruptive achromatic values (Table 4A; Fig. 4A). The
chromatic GabRat channels (A and B) also showed
significant differences between the localities (Table 4B,
4C); grasshoppers from Pedregal de San Ángel had the
lowest values for channel A, whereas grasshoppers
Figure 2. Box plots of chromatic (A) and achromatic (B)
from Tlaxcala had the lowest levels for channel B.
just noticeable differences (JNDs) between the dorsal
surfaces of female and male grasshoppers and their Interestingly, the disruptive properties of both sexes
respective backgrounds. In both cases, there are significant in Morelia were similar in achromatic and chromatic
differences according to Tukey’s HSD tests. Data were channels, although males in Pedregal and Tlaxcala had
plotted using square root transformations. more disruptive patterns than females. Moreover, we
found high and significant differences in the magnitude
those of females against their background (Table 2C; of the disruptive coloration between females and males,
Fig. 3C). The dominant markings in the background although only in channel A did we find the highest
of the localities and places where females and males and most significant differences in the magnitude of
were found were similar (Table 2D), although the the disruptive coloration between females and males
pattern diversity was higher in Morelia (Table 2E; in Pedregal de San Ángel and Tlaxcala (locality × sex
Fig. 3B), and the overall pattern contrast differed interaction), with males being more disruptive than
between the localities and places where females and females. Interestingly, in Pedregal de San Ángel,
males were located. Contrast was higher in Morelia, perhaps the most diverse chromatic environment, the
but the places where the males were found exhibited disruptive differences between females and males for
higher contrast than where the females were found GabRat channel A were higher than in the other two
(Table 2F; Fig. 3C). localities (Table 4B, 4C; Fig. 4B, C).
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911906 R. CUEVA DEL CASTILLO ET AL.
Table 2. ANOVAs of the size of the dominant marking, diversity and overall pattern contrast of the dorsal surface of the
grasshoppers (A–C) and of their background surfaces (D–F)
Source d.f. Sum of squares Mean square F-value P-value
(A) Size of dominant marking of dorsal surface of grasshoppers
Locality 1 1.82 0.91 3.21 0.043
Sex 2 22.75 22.75 80.27 > 0.0001
Residuals 151 42.8 0.28
(B) Pattern diversity of dorsal surface of grasshoppers
Locality 2 0.015 0.0077 0.855 0.427
Sex 1 0.054 0.0543 6.05 0.015
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Residuals 151 1.35 0.009
(C) Overall pattern contrast of dorsal surface of grasshoppers
Locality 2 8.1 4.05 31.23 > 0.0001
Sex 1 9.269 9.27 71.48 > 0.0001
Residuals 151 19.58 0.13
(D) Size of dominant marking of background surface
Locality 2 0.88 0.442 0.92 0.399
Sex 1 0.12 0.122 0.25 0.614
Residuals 151 72.21 0.478
(E) Pattern diversity of background surface
Locality 2 0.139 0.070 7.57 0.0007
Sex 1 0.0027 0.0026 0.29 0.59
Residuals 151 1.38 0.0092
(F) Overall pattern contrast of background surface
Locality 2 6.27 3.135 8.92 0.0002
Sex 1 3.31 3.314 9.42 0.0025
Residuals 151 53.1 0.352
DISCUSSION on achromatic signals (Osorio et al., 1999). Also,
chromatic signals could be useful in searching tasks
Our results show that females bear a closer
in variable light conditions (Schaefer et al., 2006;
resemblance to the background (colour and patterns)
Cazetta et al., 2009). Perhaps, the main predators of
than males. However, males have a higher disruptive
these grasshoppers are chromatically oriented, and
coloration than the females, showing smaller marks
this might favour chromatic background matching,
with more contrasting and diverse patterns than
whereas the achromatic signals could be less reliable
females. Interestingly, we found a different pattern in
if there are large fluctuations in daily light conditions.
Morelia. Although females bear a closer resemblance
The differences in colour pattern between the
to the background than males, the marking diversity
populations of S. purpurascens can be attributed to
of males and females is similar. The grasses generate
local adaptation to different environmental conditions.
a background composed of contrasting lights and
The differences in the selective pressures in the three
striped shadows that might favour similar disruptive
populations of S. purpurascens seem to favour the
properties in males and females. Nonetheless, despite
evolution of two cryptic strategies: disruptive markings
interpopulation differences, we found a relatively high
and matching coloration. Disruptive coloration could
chromatic background matching and resemblance
evolve in visually heterogeneous microhabitats because
to the background in grasshoppers from the three
it breaks the outline of an organism despite the variable
localities, although the achromatic background
background patterns, whereas background matching
resemblance was lower.
could be favoured in chromatically homogeneous
The differences between chromatic and achromatic
microhabitats (Robledo-Ospina et al., 2017; Orton &
channel background matching could be associated
McBrayer, 2019). The lights and striped shadows of the
with different levels of success in predator searching
grassland outside Morelia could explain the similarity
distances. Predators that search over short distances
between female and male disruptive patterns. This
or hunt large targets might rely more on chromatic
environment contrasts with Pedregal de San Ángel,
signals, whereas those that search over relatively
a place that offers a complex environment with a
larger distances or hunt small targets might rely
wide diversity of plants, which might lead to a wide
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911SEXUAL DICHROMATISM IN A GRASSHOPPER 907
heterogeneity increases the possibility that both
females and males are found in different background
patterns. In contrast, the grasshoppers from the oak
forest border in Tlaxcala show intermediate levels
of sexual dichromatism, which could be associated
with a more homogeneous and less visually complex
environment than Pedregal de San Ángel.
The marking elements associated with females
and males can be cryptic if they reduce the risk of
boundary detection by potential predators (Merilaita,
1998; Cuthill et al., 2005; Schaefer & Stobbe, 2006) and
can be adaptative in organisms with high mobility in
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heterogeneous environments (Stevens et al., 2006a, b).
This strategy is more evident in females and males
from Morelia, and is principally followed by males
from Pedregal de San Ángel and Tlaxcala. We could
expect high mobility in males because usually they
search actively for females, especially in protandrous
species (Thornhill & Alcock, 1983). Interestingly, in
Pedregal de San Ángel, the males of S. purpurascens
are protandrous (Cueva del Castillo & Núñez-Farfán,
1999), and they are also more mobile than females
(Camacho Castillo, 1999).
In Pedregal de San Ángel and Tlaxcala, females
exhibit less disruptive coloration than males, but
their background matching is higher than in males. In
these two localities, the payoff for this strategy could
be higher for females owing to the environmental
homogeneity of the places where they can be found.
The colour matching with their background could
reduce their detectability if their mobility is reduced or
if they can place themselves where the colour match
is high (Endler, 1978; Merilaita et al., 2017; Michalis
et al., 2017). However, in a heterogeneous environment
it would depend on the ability of individuals to stay in a
highly matching microhabitat or reduce their mobility
(Merilaita et al., 1999; Bond, 2007), as occurs in the
population of S. purpurascens in Pedregal de San Ángel
(Camacho Castillo, 1999). The large size of females
(Cueva del Castillo et al., 1999) and the increase in
their weight owing to egg maturation could explain
their lack of mobility. In any case, we interpreted
these results considering the human visible spectrum.
The spectral sensitivity could be very different in
other possible predators, such as birds or mice. Their
prey detectability could involve elements that we did
Figure 3. The different marking patterns measured in
not consider in this study (Théry & Gomez, 2010).
both sexes and localities. A, size of dominant marking. B,
However, humans and other potential predators of
diversity. C, overall pattern contrast. Values are presented
as the mean (SEM). Different symbols denote differences
these grasshoppers, such as mice, share part of their
between the organisms and their backgrounds according to visible spectrum (green and red) to detect potential
Table 3. prey (Denman et al., 2018), and in certain conditions,
birds and humans perform similarly in detection tasks
(Dukas & Kamil, 2001; Michalis et al., 2017).
variety of visually complex patterns (see Dimitrova In S. purpurascens, chromatic polymorphism and
& Merilaita, 2010) and where high levels of sexual sexual dichromatism could represent stable specialist
dichromatism in S. purpurascens can be found. Visual strategies (polymorphic crypsis) that have evolved
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911908 R. CUEVA DEL CASTILLO ET AL.
Table 3. Student’s paired t test comparisons of pattern parameters of dorsal surface of the different populations of
Sphenarium purpurascens grasshoppers and their background
Locality and sex Pattern variable d.f. t P-value
Morelia, female Size of dominant marking 19 −1.22 0.2371
Pattern diversity 19 0.74 0.4664
Overall contrast 19 −2.89 0.0092*
Morelia, male Size of dominant marking 19 2.91 0.009*
Pattern diversity 19 1.41 0.1733
Overall contrast 19 −7.3 < 0.0001*
Pedregal, female Size of dominant marking 25 −1.57 0.1273
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Pattern diversity 25 1.12 0.2747
Overall contrast 25 −2.51 0.0187*
Pedregal, male Size of dominant marking 30 5.55 < 0.0001*
Pattern diversity 30 −1.74 0.0917
Overall contrast 30 −6.64 < 0.0001*
Tlaxcala, female Size of dominant marking 25 −0.77 0.4489
Pattern diversity 25 −0.26 0.7953
Overall contrast 25 −3.26 0.0031*
Tlaxcala, male Size of dominant marking 31 4.54 < 0.0001*
Pattern diversity 31 −2.83 0.0081*
Overall contrast 31 −3.99 0.0003*
*P-value of P < 0.05.
Table 4. ANOVAs of the GabRat values
Source d.f. Sum of squares Mean square F-value P-value
(A) GabRat of L channel (acromatic channel)
Locality 2 3.015 1.5074 27.80 0.0001
Sex 1 0.134 0.134 2.47 0.118
Locality × sex 2 0.046 0.023 0.42 0.655
Residuals 149 8.08 0.0542
(B) GabRat of A channel
Locality 2 0.88 0.44 6.99 0.0012
Sex 1 2.18 2.18 34.60 0.0001
Locality × sex 2 1.23 0.61 9.74 0.0001
Residuals 149 9.41 0.063
(C) GabRat of B channel
Locality 2 1.52 0.76 8.51 0.0003
Sex 1 1.71 1.71 19.16 0.0001
Locality × sex 2 0.37 0.19 2.09 0.13
Residuals 149 13.28 0.089
as a result of the diversity of predators and hunting camouflage that is not perfectly background matched to a
strategies associated with environmental heterogeneity. single habitat but instead offers a degree of resemblance
Nevertheless, the differences in spectral sensitivity and to multiple backgrounds and/or using camouflage that
visual acuity of potential predators and the differences works somewhat independently of background matching
in mobility of the grasshoppers could constrain the (Hughes et al., 2019).
evolution of crypsis (Caves et al., 2018; Hughes et al., Our results might have important implications
2019). The chromatic patterns of the grasshoppers could regarding the origin and maintenance of intraspecific
be generalist (or compromise) strategies that might colour variation with respect to selection pressures
match several backgrounds to some extent, but none imposed by visual predators. We are currently
closely. These grasshoppers might be adopting a form of conducting studies on predation and escape behaviour
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2021, 132, 900–911SEXUAL DICHROMATISM IN A GRASSHOPPER 909
ACKNOWLEDGEMENTS
This research was supported by the project PAPIIT-
UNAM IN211617. Víctor Hugo Ramírez-Delgado
acknowledges the Posgrado en Ciencias Biológicas
of the Universidad Nacional Autónoma de México
(UNAM) and Consejo Nacional de Ciencia y Tecnología
(CONACyT) for a doctoral scholarship (no. 330551).
The authors wish to thank M. A. Serrano-Meneses
and Salomón Sanabria-Urbán for their help in the
field, and Judith X. Ponce-Wainer for her valuable
suggestions to improve the quality of the manuscript.
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Valuable suggestions on the manuscript were made by
two anonymous reviewers and the editor.
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SHARED DATA
The data of the study are available from the Zenodo repository: https://zenodo.org/record/4330018#.X9uvmGm73qs.
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