Acta Oecologica 37 (2011) 93e98
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Original article
Adaptive colour polymorphism of Acrida ungarica H. (Orthoptera: Acrididae) in a spatially heterogeneous environment Loïc Pellissier a, *, Jérôme Wassef a, Julia Bilat a, Gregory Brazzola a, Pierrick Buri a, Caroline Colliard a, Bertrand Fournier b, Jacques Hausser a, Glenn Yannic a, Nicolas Perrin a a b
Department of Ecology and Evolution, University of Lausanne, Bâtiment Biophore, CH-1015 Lausanne, Switzerland Laboratory of Soil Biology, University of Neuchâtel, CH-2009 Neuchâtel, Switzerland
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 October 2010 Accepted 13 December 2010 Available online 13 January 2011
Intra-specific colour polymorphism provides a cryptic camouflage from predators in heterogeneous habitats. The orthoptera species, Acrida ungarica (Herbst, 1786) possess two well-distinguished colour morphs: brown and green and displays several disruptive colouration patterns within each morph to improve the crypsis. This study focused on how the features of the background environment relate to the proportion of the two morphs and to the intensity of disruptive colouration patterns in A. ungarica. As the two sexes are very distinct with respect to mass and length, we also distinctively tested the relationship for each sex. In accordance with the background matching hypothesis, we found that, for both sexes, the brown morph was in higher proportion at sites with a brown-dominant environment, and green morphs were in higher proportion in green-dominant environments. Globally, individuals in drier sites and in the drier year also had more intense disruptive colouration patterns, and brown morphs and females were also more striped. Colour patterns differed largely between populations and were significantly correlated with relevant environmental features. Even if A. ungarica is a polymorphic specialist, disruptive colouration still appears to provide strong benefits, particularly in some habitats. Moreover, because females are larger, they are less able to flee, which might explain the difference between sexes. Ó 2010 Elsevier Masson SAS. All rights reserved.
Keywords: Background matching Crypsis Disruptive colouration Aposematism Camouflage
1. Introduction Prey species have evolved a large diversity of strategies to limit predation, among which the most common are active escape and cryptic colouration (Forsman and Appelqvist, 1998). Which strategy evolves in a specific context will depend on the habitat background as well as on the biological constraints of the organism (e.g., mass, body shape, flight organs). The various evolved strategies, however, are not mutually exclusive alternatives: many grasshopper species, for instance, have developed in parallel both an efficient crypsis and the ability to escape by jump or flight once discovered. Crypsis, i.e., resemblance to the background environment, can be achieved either by general background matching (Ahnesjo and Forsman, 2006; Stevens and Merilaita, 2009) or by disruptive colouration (Silberglied et al., 1980; Stevens and Merilaita, 2009). In the case of background matching, individuals evade predation by mimicking the colour or other features of the environment they inhabit. As a consequence, predators that hunt by sight have greater * Corresponding author. Fax: þ41 21 692 42 65. E-mail address:
[email protected] (L. Pellissier). 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.12.003
difficulty distinguishing prey from the background. Hence, the efficiency of crypsis should depend on the degree of resemblance of the prey’s colouration to the background features. For example, Fuller and Joern (1996) showed experimentally that grasshopper species tend to be less susceptible to predation in areas that are most similar to their naturally chosen microhabitats, and Ahnesjo and Forsman (2006) found that different genetic colour morphs of the pygmy grasshopper, Tetrix undulata, select substrates that reduce predation risks. Apart from background matching, a large number of grasshopper species display variation in points and stripes along the body, called disruptive colouration, which improves their camouflage by breaking up the body into a series of apparently unrelated objects (Cott, 1940; Silberglied et al., 1980; Sandoval, 1994; Stevens and Cuthill, 2006; Stevens and Merilaita, 2009). Because the combination of disruptive colouration and crypsis works better than either one alone, disruptive colouration is an efficient improvement to the crypsis by background matching (Cuthill et al., 2005; Stevens et al., 2006). Additionally, a disruptive pattern alone can have a significant effect independently from colour morph (Schaefer and Stobbe, 2006).
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Disruptive colouration works on a higher diversity of visual backgrounds than background matching, and, thus, it might allow greater survival in heterogeneous habitats and enable individuals to forage in more diverse places (Ruxton et al., 2004; Sherratt et al., 2005). This is highly advantageous compared to developing a unique strong crypsis which reduces the risk of predation but constrains the prey species to a very few specialized habitats (Merilaita et al., 1999; Ruxton et al., 2004). Crypsis in a heterogeneous habitat may be achieved by compromising the degree of crypsis between diverse microhabitats and alternatively improving it in one of the microhabitats at the expense of the others (Merilaita et al., 1999). Or it may be achieved more efficiently by developing intra-specific, locally adapted polymorphisms (Eterovick et al., 1997). Colour polymorphism, however, may also be maintained by predation through aposematism. Predators may build a search image of the most common prey, which should provide frequencydependent benefits for rare morphs (Rand, 1967). This selective attention leads to frequency-dependent selection, favouring rarer forms and, thus, maintaining polymorphism (Bond, 2007). These two mechanisms differ in several aspects. Apostatic selection relies crucially on genetic polymorphism, and it maintains diversity at a within-habitat scale through frequency-dependent selection (independently of the habitat background). In contrast, the polymorphism maintained by spatial heterogeneity may also rely on phenotypic plasticity. In this case, polymorphism will mostly accrue among habitats, such that colour patterns are expected to co-vary with environmental features. Patterns of covariance, however, should be modulated with specific behaviours, particularly by patterns of dispersal among populations, as well as by the active search of cryptic microhabitats. In particular, prey should favour areas in which their colouration confers strong crypsis (Ergene, 1952; Sandoval, 1994; Eterovick et al., 1997; Ahnesjo and Forsman, 2006) while avoiding habitats where they have low performance. For example, the larvae of Acrida turrita have been shown to prefer habitats matching their body colour (Ergene, 1952). The current study investigates the colour-morph and disruptive-pattern polymorphisms in Acrida ungarica (Herbst, 1786) in a heterogeneous habitat. This species presents two distinct colour morphs (green and brown), both showing a continuous variance in disruptive colouration levels. We tested whether to proportions of
the two colour morphs varies with environments (expressed in terms of vegetation composition, aspect and cover) and with sex. We also investigated the variation of the intensity of disruptive colouration according to the environment as well as to the sexes and morphs of the individuals. From the background matching hypothesis, we expected 1) The variance in colouration would take place among, rather than within, populations. 2) The among-population variance would be correlated with environmental features, and, in particular, the proportion of brown morphs would increase with the dominance of brown grasses and bare soil. 3) The relationship in females would be greater than in males because owing to their larger size, they are more profitable to predators, less cryptic, and less able to escape by flight.
2. Methods 2.1. Target species Acrida ungarica (Acrididae, Orthoptera) is a large grasshopper living in open grasslands of Southern Europe and two subspecies are actually recognized: Acrida u. ungarica from south-eastern Europe and Acrida u. mediterranea in south-western Europe (Harz, 1975). With a total length of 65e75 mm from the head to the end of the wings, females are much larger than males (35e45 mm). Two colour morphs, green and brown, are distinguished, and the wings and the body of individuals have varying levels of disruptive colouration, which mainly comprises stripes and dots of different intensities of black, pink and white (Fig. 1). 2.2. Study area and field sampling Our study sites are situated on the Bulgarian shore of the Black Sea in south-eastern Europe. Several types of grassland occur there, and the type of grassland varies according to the soil properties and the availability of water to the vegetation. We classified grasslands into three categories: 1) sand meadows, vegetation associations on drained sand dunes and beaches characterised by the presence of
Fig. 1. Pictures of two females of Acrida ungarica in their habitats where they are most cryptic: the brown morph (a.) and the green (b.). The patterns of disruptive colouration are also distinguishable along the body of the two individuals (Pictures credit: Nicolas Perrin) (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.).
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Artemisia maritima and Centaurea arenaria, 2) shore meadows, denser vegetation occurring near the shore of the sea but with a richer type of soil characterised by the occurrence of the thermophilous species Brachypodium ramosum and the halophytic Limonium gmelinii and 3) moist meadows, mesophile grasslands and pastures possessing a deep and nutrient rich soil with graminoids such as Festuca pratensis, Poa pratensis or other species such as Plantago lanceolata. The dryness and cover of bare soil differs greatly between the three vegetation types. The sampling was conducted in the two first weeks of September 2006 and 2007. During the first year, 12 sites were visited (5 moist meadows, 4 shore meadows and 3 sand meadows) and in the second year, 14 sites were visited (6 moist meadows, 4 shore meadows and 4 sand meadows). The weather conditions were consistently fine and sunny during both field seasons (mean T C 2006: 18.9 C and 2007: 19.1 C and precipitation: 20.83 mm in 2006 and 35.82 mm in 2007). Each year, the sites were selected among grasslands belonging to the three vegetation types described above, where sites were separated by distances over 200 m. This threshold was chosen based on prior observations of daily dispersal distance of individual by mark-recapture. Individual of this species tend to have high site fidelity (Personal observation). The final average distance between sampled sites is 5.8 km. In each meadow, we estimated the proportion of cover by green grasses, brown grasses. Bare soil was only recorded in 2006. We laid four 10 m by 10 m plots in the inventoried grasslands in order to better visualise the covers of these features and finally averaged the proportions estimated in the four plots. Grasshoppers were captured by nets during one-hour random walks, and they were temporarily stored in plastic boxes in order to avoid recapture. After one hour, the sex, colour morph (green or brown) and intensity of points and stripes (scale ranging from 0 to 5, Table 1) were recorded for all individuals before release. Individuals were picked randomly (independent of sex or morph) from the plastic boxes and scored by one of the fieldworkers, using a dataset of reference. Since the scores were attributed in total by eight people randomly after thoroughly discussing the visual criteria, it is unlikely to lead to inconsistent scoring and bias in the following analyses.
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the total number of captured individuals) per site to the categorical variable of vegetation type (three categories) as a fixed effect and year as a random effect. We also related the proportion of brown morphs to the continuous variable of the proportion of brown grass in the inventoried sites. Since the two sexes are very different from each other as regards to mass and length, we also tested the relationship between the proportions of brown morphs of each sex to the proportion of brown grass. These models were run with the lme4 package (Bates et al., 2008) implemented in the R environment (R development core team, 2009). The likelihood was computed using the Laplace approximation as recommended by Bolker et al. (2009). The proportion of total brown morphs and brown morphs of each sex were also related to the cover of bare soil (in 2006) using a generalised linear model (GLM, McCullagh and Nelder, 1989) with a binomial distribution and a logistic link function. Using a linear mixed model (LMM) with a normal distribution, we related the average score of intensity of disruptive colouration patterns per site (continuous variable) to the proportion of brown grass as a fixed effect and the year as a random effect. By taking the average score of intensity of disruptive colouration patterns per site, we both capture the general trend in each population and transform the discrete scores into a continuous variable. This model was also run using the lme4 package (Bates et al., 2008). We assessed the assumption of normality with the normal probability plot of residuals (Pinheiro and Bates, 2000). The results did not indicate any departure from normality. The likelihood was computed using Markov chain Monte Carlo with a function implemented in the langageR package. Finally, we compared the average scores of intensity of disruptive colouration patterns per site between sex and morph with paired student’s t-tests, i.e. by comparing the average scores two by two within each site which allow dealing with the effect of year. We also assessed the assumption of normality with the normal probability plot of residuals also showing no departure from normality. While using rank-based methods directly on the values of the individuals might be a more straightforward approach, this would not allow dealing with the random effects of year but also of site arising.
2.3. Statistical analyses Using generalised linear mixed models (GLMM) with a binomial distribution and a logistic link function, we related the proportion of brown morphs (i.e. number of brown individuals compared to Table 1 Scale used to score the intensity of colouration of the two morphs, green and brown, of A. ungarica. Intensity
Description
0 1 2
Plain colour, green or brown Darker thorax keel Darker thorax keel spotted with brown and black; beginning of black lines on the wings Darker thorax keel spotted with brown and black; beginning of black lines on the wings; beginning of black stripes flecked with white marks on the sides of the body Darker thorax keel spotted with brown and black; brown and rose line under the keel; beginning of black lines on the wings; beginning of black stripes flecked with white marks on the sides of the body Very dark thorax keel spotted with brown and black; brown and rose line under the keel continuing on the wings; black lines on the wings; black stripes highly contrasting with white marks on the sides of the body and on the wings
3
4
5
3. Results Overall, 1147 individuals were sampled during the two years (see Appendix S1), among which 560 individuals were sampled in 2006 (332 males and 228 females) and 587 individuals, in 2007 (372 males and 215 females). The green colour morph was generally more frequent (75e79%) except in males for the year 2007, when the two morphs were equally present (48% green). The proportions of the two morphs differed significantly between vegetation types (Table 2), with the brown morph being proportionately lower in moist meadow and higher in sand meadows. Accordingly, the proportion of brown morphs also increased significantly with the proportion of brown grass and inversely for the proportion of green morphs (Table 2; Fig. 1) and bare soil (Table 2). Both relationships were also significant when the sexes were analysed separately, though the relationship was less significant for females (Table 2) (Fig. 2). The average intensity of disruptive colouration varied significantly between morph, sex, and in relation to the proportion of brown grasses (Table 2). Females were more striped than males, the brown morph was more striped than the green morph, and the intensity of disruptive colouration increased with the proportion of brown grasses (Fig. 3).
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Table 2 Results of the statistical analyses: GLMMs of the proportion of brown morphs, GLM of the proportion of brown morphs in relation to bare soil for 2006 only, LMM of the intensity of disruptive colour for 2006 and 2007, and finally t-tests comparing the intensity of disruptive colour between sex and morph. Response variable
Explaining variable
GLMM1 GLMM2 GLMM3
Proportion of brown male Proportion of brown female Proportion of brown
Proportion of brown grass Proportion of brown grass Proportion of brown grass
0.036 0.023 0.033
7.45 3.7 9.98
