Sexual Dimorphism in Physiological Reactions to Biotope Type (the Case Study in Ground Beetles)

Abstract

Sexual size dimorphism (SSD) (the difference between males and females in size) is considered to be the physiological reaction to environmental conditions. We estimated body size variation and SSD in two populations of ground beetle Carabus exaratus. Beetles were sampled in Krasnodar Province (Russia) in the forb-cereal meadow and beech-hornbeam forest. We processed morphometric measurements in 521 specimen for six linear traits. Beetles from the meadow were slightly larger than from the forest. SSD was pronounced in a half of traits being the highest by elytra length. On a whole, SSD did not differ in the populations studied.

1. Introduction

A lot of studies deal with the relationships between the sizes of different parts or entire bodies of organisms. They investigate how such body size variation affects different morphologies and important functions, that is, physical strength, metabolic rates, and transport of resources [1]. Such size patterns can be studied both within individuals and species and across species of plant or animal. Male and female insects often differ morphometrically, by size [2]. Females are usually larger than males, while males demonstrate lower phenotypic plasticity [3, 4]. Phenotypic plasticity is induced by ecological and environmental variables.

The aim of our study was to top up the knowledge in sexual size dimorphism (SSD) in insects, specifically in ground beetles. The former studies showed SSD variability in these beetles depending on environmental conditions. We chose Caucasian species 0 Carabus exaratus Quencel, which was not sufficiently investigated. So we hypothesized that: (i) SSD in it is female-biased; (ii) the beetles from different biotopes will differ in body size; and (iii) SSD by different traits will vary and will be the highest by elytra width.

2. Materials and methods

2.1 Object of investigation

C. exaratus is large (22–28 mm) beetle with elongated body and long legs. It is distributed from foothill steppes till subnival zone. Dominates at foothills in North-Eastern Caucasus and plain parts of Ciscaucasia [5]. Recorded in Rostov and Krasnodar Provinces. Generalist, forest-meadow species, predator with spring-summer breeding.

2.2 Sampling area

We trapped beetles in two biotopes at Krasnodar Province, Tuapse district, Russia. The first biotope was forb-cereal meadow (44.3833°N 38.9667°E, 550 m asl), periodically used for Zea mays L. and Solanum tuberosum L. cultivation and grazing. The second one was beech-hornbeam forest in Maliy Pshish rever valley (44.1561°N 39.5279°E 520 m asl). Beetles were sampled in 2018 and transported to Laboratory of Biomonitoring Institute for Problems of Ecology and Mineral Wealth Use of Tatarstan Academy of Sciences for measuring. Presented work is the fragment of the investigations in our laboratory. Beginning from 1996, we sampled ground beetles in different regions of Russia and abroad. Beetles are sampled by professional carabidologists for their own purposes and then are posted to our laboratory for the morphometric analysis, because the main aim of our investigation is the clarifying ecogeographical rules (Bergmann, Rensch ets.). So we have to process material in male and female body size variation in latitude and longitude gradients. Thus, samples from the region mentioned (Krasnodar Province) were the part of the material we need to fulfill our aims.

2.3 Morphometric analysis

Nikon D5100 camera was used to get images of beetles. We acted according to the methodology approved in our laboratory, since morphometric analysis requires certain skills and must be carried out by permanent employees. We measured them using a program. The latter was written specifically for the given method of measurement and utilized a distance between manually pointed out elements of photo arrays as the terminal point of measurements and the fiducial scale. Initial codes from the program are available under the free permissive license MIT [6]. Six traits were under investigation: the length and the width of elytra, pronotum, and head. In total, 480 specimens were measured.

2.4 Statistical analysis

Statistical analysis was done using Excel programs. Sexual Size Dimorphism (hereinafter SSD) was calculated as follows: mean value of trait in females/mean value of trait in males-1 [7].

3. Results and discussion

SSD in ground beetles is female-biased [8]. It is common for the vast number of species in invertebrates. The value of SSD is not constant because phenotypic plasticity of body size can vary substantially between the sexes and can cause intraspecific variation [9]. The most interesting opinion on SSD was expressed in Evolutionary Theory of Sex [10]: Males are the vanguard of evolution. They are more variable than females and become very variable in unusual conditions. Purely mathematically, this leads to the reduction of differences between males and females. So in severe environment SSD values increase. On the contrary, in stable environment, without any destabilizing effects, SSD will decrease. Some studies in ground beetles confirmed that suggestion. In mountain populations of ground beetles Carabus odoratus Schill. and Pterostichus montanus Motsch. SSD highly correlated with population number [11]. It is well known that these conditions lead to resources lack, stress etc. And exactly in those severe conditions SSD in those populations was high. In relation to C. exaratus, the highest values in SSD were recorded in severe conditions of high mountains [10]. In our study, the situation was somewhat another. We recorded SSD not by all traits investigated (Figures 1 and 2): In elytra length SSD was pronounced in both biotopes, but it was not recorded in elytra width, and was male-biased by pronotum length in the meadow population, and was not recorded in pronotum width and head parameters in the forest population of C. exaratus.

Figure 1.

Elytra length variation in C. exaratus.

Figure 2.

Traits value variation in C. exaratus.

Those facts evidenced that environmental conditions were quite stable in area studied. Probably estimated biotopes differed slightly in food resource procuring. Beetles were slightly larger in the meadow, and larva nutrition is considered the main factor that impacts imagoes size. Ground beetles are largely predators feeding on soil micro- and macrofauna representatives—microbes, Formicidae, Silphidae larvae, small species of Staphylinidae, Coccinellidae, Dermestidae, larvae of Lepidoptera, Hemiptera, Thomisidae, Opiliones, and Lumbricidae [12, 13]. Sometimes, carabids consume their “relatives,” for example, Pterostichus melanarius Ill. fed readily on Stomis pumicatus (Panzer, 1795), Harpalus amplicollis Mentries, 1848, Panagaeus bipustulatus (Fabricius, 1775) [14]. Distribution of ground beetles preys is spatially very diverse. This fact can explain biotope impact on beetle size variation. In arable lands of Europe, the size in ground beetle Poecilus cupreus L. in rye differed greatly from the crops. The authors correlated with that fact to the peculiarities of rye cultivation: strong root system and shallow seed embedding. Besides, beetle body size and their shape differed in the crops with heavy above-ground parts (carrot, pea, vetch, and oat) and rarefied ones (lawn, meadows) [15]. In Carabus granulatus L. beetles were larger in the meadows, but significantly smaller in oak and elm forests if compared with birch ones [16]. Such the differences are based on the different litter decomposition in cited biotopes, where carabid preys dwell [17].

In our case, the beetles in the forest and at the meadow did not differ in size significantly (except their elytra width). This, to our mind, means that the place in area should be taken into account too when exploring body size variation in different populations of ground beetles [18, 19]. For several species of carabids, the distinct curves of size variation were shown in latitude gradient [19] and often males and female response to latitude gradient differed [20, 21]. The plots we explored were situated in nearby locations, so they did not differ significantly in weather conditions and climate in a whole. The latter also affects ground beetle size variation [22, 23].

Besides real size variation the variation of shape should be studied. Our investigated species—C. exaratus—showed distinct shape variation in altitude gradient with elongated specimen in low mountains [24].

As for sexual size dimorphism the samples we studied followed the established rule that SSD in carabids is female-biased [25] females being larger than males. On a whole when considering all traits we did not find significant differences in SSD value in the meadow and forest populations (Figure 3).

Figure 3.

Sexual size dimorphism (as the mean by all traits investigated) in C. exaratus.

In any way our findings contribute greatly into our knowledge in SSD variation in both carabids and insects. Intra-specific level of investigation allows us to frame mechanisms of body size variation in different habitats and in different sexes. The latter highlight ways of SSD evolution. And it is sufficiently important as SSD is considered to be the indicator of environmental quality.

As mentioned in Material and Methods we are presenting here the fragment of our large study. In previous papers, we put forward the hypothesis that body size variation in ground beetles is genera-specific in latitude gradient: In Carabus beetles, the curve monotonically falls northwards but in Pterostichus ones it is saw-tooth. The latter can be explained by life-cycle changes. As for studied C. exaratus, we have the only one region else to be compared with Krasnodar Province—Chechen Republic [10]. The following step of our studies will include comparative analysis of this species samples from different regions and replenishment of our dataset with new data.