Introduction

The ecological region of the temperate forest of southern Chile has a long history of geographic isolation, generating a narrow distribution range and high levels of endemism in its biota, which has been unaffected by anthropogenic disturbance since the Quaternary. Unfortunately, for more than 70 years the Aysén Region has been subject to several events that have endangered its biodiversity, especially extensive burning of forests, use of land for agriculture and animal husbandry, and, more recently, colonization (Espinoza et al. 1994, Quintanilla 2008). As a result, the landscape, particularly in the southern part of the region, has been dramatically modified from its original state.

Floate and Fox (2000) and Piscart et al. (2005) have shown that the degrees of phenotypic disturbances reflect the ability of an individual to overcome the effects of stress, suggesting that more symmetrical individuals would have a greater survival probability than those with high levels of asymmetry. However, because of adaption over time to a specific environment, environmental pressures and geographic distances affect geographic microenvironments locally and thus their associated flora and fauna (Alibert et al. 2001; Cepeda-Pizarro et al. 2003; Benítez et al. 2008). There is evidence that temperatures, adverse nutritional stress, chemical presence, density of population and many other factors causing stress during development can lead to increased fluctuating asymmetry (e.g. Rettig et al. 1997; Benitez et al. 2008, Henríquez et al. 2009; Benitez et al. 2010b). Therefore, it is expected that when environmental conditions change, organisms and populations should adapt to the new conditions (Clarke 1993). As a consequence, the generation of symmetric phenotypes is conditioned by the dampening of the phenotype in response to the disturbances that occur during morphogenesis (Labrie et al. 2003; Leamy and Klingenberg 2005).

Ceroglossus is a genus of carabid beetles endemic to the forests of southern South America that include eight species: the Chilean magnificent beetle, C. chilensis (Eschscholtz) (Coleoptera: Carabidae), C. darwini (Hope), C. speciosus Gerstaecker, C. magellanicus Géhin, C. buqueti (Laporte), C. suturalis (Fabricius), C. ochsenii (Germain), and C. guerini (Germain), all of diurnal habit and predators on smaller organisms.

A marked chromatic polymorphism has been found in populations of Ceroglossus, which may be associated with environmental differences like temperature and humidity (Jiroux 2006). This has been corroborated in C. chilensis with DNA analysis (Okamoto et al. 2001).

*Dense activity: temporal and spatial variations of relative abundance, determined by the effect they have some atmospheric variables on activity and the presence of barriers that limit their free movement

C. chilensis has 26 subspecies, distributed from the Maule Region and the extreme south of the Aysén Region; it is also present in Argentina, and is the southernmost species and the one with the widest distribution in Chile. It prefers more xeric habitats and is more tolerant of arid conditions than its congeners. It is not known if its size, which is relatively large for a carabid, is related to its ability to resist the aridity of the environment (Jiroux 2006). There is evidence that the development and environmental instability of C. chilensis, a species with a high activity density, is affected by the modified environment versus the natural environment (Briones and Jerez 2007; Benitez et al. 2008, Henríquez et al. 2009).

The Baker River Basin has the largest water volume of any river in Chile; it is 200 km long, drains an area of 26,487 km² and has its origin in Lake Bertrand. In the Baker River Basin, C. chilensis is found in mixed mature evergreen forests containing Nothofagus dombeyi Mirbel (Ørsted) (Fagales: Nothofagaceae) and N. nitida Hofmus, and in second-growth forests containing N. pumilio (Poeppig et Endl.) Krasser (Rodriguez et al. 2008). There is an approximate distance of 85 km isolating these two habitats (Benitez 2008), an area that is populated by diverse vegetation types from anthropogenic intervention, exotic plantations, grasslands, antarctic beech forests of Nothofagus antartica (G. Forster) Oerst, and shrublands with Embothrium coccineum J.R. et G. Forster (Proteales: Proteaceae). Therefore, since the same insect species exist in these two geographically isolated environments, we may expect to find different morphotypes as a response of this species to the different environmental disturbances occurring particularly in each of these sites.

Table 1.

Anatomical description of 28 external landmarks in Ceroglossus chilensis body shape.

The objective of this study was to evaluate the morphological differentiation and the sexual dimorphism within and between populations of C. chilensis in different and isolated geographic areas of the Baker River Basin, using geometric morphometric.

Materials and Methods

Results

We collected a total of 477 individuals of C. chilensis, 148 males and 140 females in mature forest and 96 males and 93 females in second-growth forest. The high activity density (sensu De los Santos et al. 2002) for mature forests indicates 12.8 ind/trap and 3.5 ind/trap for second-growth forest. The Mantel test applied to the data of high activity density, indicated that sampling units are not spatially auto-correlated and are statistically independent. This indicates that there is no significant relationship between the differences of high activity density (p = -0.25) of C. chilensis and their spatial separation.

To quantify body size, we used centroid size, which is a measure of the spread of landmarks around their centre of gravity (Dryden and Mardia 1998). A multivariate regression for the variable shape and centroid size, plus a generalized Goodall F test (F = 7.8223; df = 52. 2189; p < 0.0001) discounted the presence of an allometric factor; there were not large differences between the first axis of the principal components (shape variables and the logarithm of centroid size).

Non-uniform variations (k-3 principal warps, where k is the number of landmarks) were calculated for mature forest (F) and second-growth forest (S). The deformations were calculated with the first and last principal warps, with which the global changes for F had a folding index of λ = 5.2599E-007 and λ = 0.0001855 for local changes, while S had global λ = 6.0965E-007 and local λ = 0.0001819. The global changes were similar for both formations.

Discussion and conclusions

The variation in shape of C. chilensis was clearly demonstrated by the techniques of geometric morphometric. Although there were differences in shape and size between forests and second-growth forest, these were less different among the sites within each type of vegetal formation. The maximum distance between sites was 85 km (F1 and S3) (Benitez 2008), thus it is feasible that the differences in shape, in addition to being local differences, are due at least in part to the fragmentation of the habitat (Henríquez et al. 2009).

Our results indicate that morphological variations and the variation among sampling sites are due to differences in shape, not to size (Adams and Funk 1997). Alibert et al. (2001) suggested that size variations among populations are necessarily influenced by the environment. However, the disturbances generated by anthropogenic activity have had a historic influence in the Aysén Region, generating a highly heterogeneous vegetation landscape.

The results of this study show that C. chilensis has only a small amount of morphological variation among sites of the same vegetation type, but have formed discrete units as a result of isolation between mature forest and second-growth forest.

Although these variations are not visible to humans by ocular inspection, they may be sufficient to produce sexual selection by the insects. The variation in the abdomen was greater in females; this is an essential morphological character which allows a female to produce more eggs and therefore have a greater fecundity and greater fitness (Andersson 1994; Cepeda-Pizarro et al. 1996; Benítez et al. 2010a; Benítez et al. 2010b).

Although there were significant differences in size among populations, we cannot argue that these are only due to sexual dimorphism. It is frequently suggested that size variation of individuals may be strongly dependent upon unfavorable environmental conditions (Adams and Funk 1997; Tatsuta et al. 2001). Thus we conclude that the differences between sexes and among sampling sites are significant for the studied vegetation types. The differences between sexes raise the question of how morphological variation and sexual dimorphism may be affected spatially as a result of natural selection.

Figure 1.

Map of Chile and the Aysén Region, indicating the study area and the sampling sites. Circles: Second-Growth Stand, Squares: Forest. High quality figures are available online.

Figure 2.

Ceroglossus chilensis. Indication of 28 landmarks in the ventral view. High quality figures are available online.

Figure 3.

3D bar dispersion plot showing distributions of the shape for males and females in the sampling sites for Mature Forest (F) and Second-growth forest (S). *M (males) * F (females). High quality figures are available online.

Figure 4.

3D dispersion plot showing the relative positions of the different sizes and sexual dimorphism in Mature Forest. The deformation grids indicate a mean shape variable for males and females. High quality figures are available online.

Figure 5.

3D dispersion plot showing the relative positions of the different sizes and sexual dimorphism in Second-growth forest. The deformation grids indicate a mean shape variable for males and females. High quality figures are available online.