In lowland areas of the world and high-altitude European mountains, the species compositions, body sizes, and wing forms of carabid beetles are known to change according to vegetation structures. However, little is known regarding the assemblage structure and habitat associations of carabid beetles in Japanese alpine-subalpine areas. We surveyed carabid beetles in four habitats (snow beds, alpine meadows,
Mountain areas are generally characterized by harsh and unpredictable environments with low temperatures, strong winds, abundant snow, and changeable climates [
Coleoptera are among the most numerically dominant mountain insects in many parts of the world [
The growing literature from lowland and mountain areas suggests that the abundance, species richness, and species composition of carabid beetles have been shown to change across habitats characterized by different vegetation structures, such as the presence of a tree canopy or forest type [
In recent years, global climate change has threatened mountain habitats and their organisms in many parts of the world. For example, in European mountains and the Andes, the distributions of vascular plants and carabid beetles have shifted toward higher altitudes [
The objectives of this study were to investigate the assemblage characteristics and habitat associations of carabid beetles in the alpine-subalpine zone of a Japanese mountain. We tested two hypotheses. First, we tested whether the carabid beetles on a high mountain were associated with specific habitats, characterized by variation in vegetation structure and microclimate. Specifically, we hypothesized that the presence of
We conducted field surveys in the upper alpine-subalpine zone (altitude 2070–2600 m) on Mt. Hakusan in Ishikawa Prefecture, central Japan (36°09′N, 136°46′E; Figure
Maps showing the location of the study area and the 11 study sites encompassing four habitats in the alpine-subalpine zone on Mt. Hakusan in central Japan (Geospatial Information Authority scale of 1/50,000; Japan Topographic Map). Murodo-daira indicates the location of the meteorological station.
We selected two or three sites in each of four habitats for a total of 11 sites. To eliminate the influence of adjacent habitats, each site was selected from the center of the respective habitat type, with each site located more than 200 m from the others. We categorized the habitats with reference to a vegetation map of 1/25,000 [
We sampled carabid beetles six times on July 15 and 24, August 13 and 27, and September 11 and 23 in 2014 using baited pitfall traps made of polypropylene cups (diameter 9 cm, depth 7 cm). Sushi vinegar and powdered silkworm are baits commonly used in Japan to collect carabid beetles [
At each site, we placed 20 traps about 2 m apart along an arbitrarily designated 38 m line. We alternated sushi vinegar (10 mL/trap) and powdered silkworm (10 mL/trap) traps along the 38 m line. Therefore, there were 10 traps of each type at each site. We set up all of the traps from 8:00 to 12:00 of the same day. The following morning, 24 hours after the start of trapping, we emptied the traps and collected the carabid beetles. In the laboratory, we identified the carabid beetles to species using taxonomic keys [
We selected six environmental variables that might affect the species richness, abundance, and assemblage composition of carabid beetles on Mt. Hakusan: soil water content, mean substrate size, ground surface temperature, diurnal temperature range, vegetation cover, and
Using a portable soil water sensor (TDR-341F; Fujiwara Scientific Company, Tsukuba, Japan), we measured soil water content by inserting the probe to 5 cm depth from the soil surface. At each site, we arbitrarily took 10 readings to determine the mean soil water content. Subsequently, we placed two parallel 5 m tape measures horizontally (5 m apart) along the slope near the center of each site. We divided each 5 m line into 10 equidistant points. We used a ruler to determine the mean substrate size at 20 locations at each site. Prior to starting the first carabid beetle sampling, we placed a data logger (HOBO TidbiT v2; Onset Computer, Bourne, MA, USA) at the center of each site. Based on hourly temperature data collected from 13:00 to 12:00 the following day, we calculated the mean ground surface temperature and diurnal temperature range of the ground surface (the difference between the maximum and minimum temperatures). We visually estimated the percentage coverage of all vegetation and
At each sampling session, we measured soil water content, mean ground surface temperature, the temperature range, and the percentage coverage by vegetation. We recorded mean substrate size and percentage coverage by
We used factorial repeated measures analysis of variance (ANOVA) or one-way ANOVA to explore differences in six environmental variables (soil water content, mean substrate size, ground surface temperature, diurnal temperature range, vegetation cover, and
We used generalized linear model (GLM) analyses to identify differences in the total carabid beetle abundance and species richness among the four habitats. We treated habitat and day as fixed factors and day as a repeated measure. We used a negative binomial model (log link) for total carabid abundance and a Poisson model (log link) for species richness data. When a habitat effect or habitat × day interaction was statistically significant (
To explore differences in species compositions among the four habitats, we subjected all daily data and the pooled data from the six samplings to nonmetric multidimensional scaling (NMDS). NMDS is an ordination technique that depicts the configuration of samples in a specified number of dimensions based on the dissimilarity matrix and iterative algorithm [
We used the biota-environment (BIO-ENV) analysis to identify environmental variables that best explained the carabid beetle compositions. The BIO-ENV analysis uses all available environmental variables to identify the combination that best explains patterns evident in the biological data. In the BIO-ENV procedure, correlations between the dissimilarity matrices of species (based on Bray-Curtis dissimilarity) and environmental variables (based on Euclidean distance) are calculated [
We performed the repeated measures ANOVA and GLMs in SPSS ver. 21 (IBM, New York, USA) and the NMDS, ANOSIM, and BIO-ENV analyses in Primer ver. 7 (PRIMER-E, Auckland, New Zealand).
Of the six environmental variables, the soil water content, mean substrate size, diurnal temperature range, and percentage coverage by vegetation differed significantly among the four habitats (Habitat: all
Soil water content (a), ground surface temperature (b), diurnal temperature range (c), vegetation cover (d), mean substrate size (e), and
Overall, snow beds were characterized by relatively high soil water content, large mean substrate size, high mean ground surface temperature, large diurnal temperature range, and high percentage coverage by vegetation (especially on August 13 and thereafter (Figure
We collected 997 carabid beetles of 23 species (Table
Total and measured sample numbers, mean body lengths (±SDs), size classes, and wing forms of carabid beetles in the alpine-subalpine zone on Mt. Hakusan in central Japan.
Species | Total samples (number) | Measured samples (number) | Mean body length ± SD (mm) | Size class | Wing form |
---|---|---|---|---|---|
| 102 | 80 | | L | ap |
| 2 | 2 | | L | ap |
| 9 | 8 | | S | ap |
| 16 | 14 | | S | br |
| 3 | 3 | | M | ap |
| 3 | 2 | | M | br |
| 3 | 2 | | S | ap |
| 10 | 10 | | S | ap |
| 15 | 14 | | S | ma |
| 459 | 369 | | S | br |
| 1 | 1 | | M | ma |
| 2 | 2 | | S | br |
| 46 | 44 | | S | br |
| 131 | 88 | | S | ma |
| 80 | 60 | | M | ap |
| 10 | 10 | | M | ap |
| 45 | 36 | | M | br |
| 47 | 40 | | M | ap |
| 1 | 1 | | M | ap |
| 7 | 7 | | S | ap |
| 2 | 2 | | S | ap |
| 2 | 2 | | S | ma |
| 1 | 1 | | M | br |
S, <10 mm; M, 10–20 mm; L, >20 mm; ma, macropterous; br, brachypterous; ap, apterous.
The mean body length of the 23 carabid beetle species ranged from 3.6 mm (
Of the 23 carabid beetle species identified in the study, only four species (
GLM did not reveal a significant habitat × day interaction in the total carabid beetle abundance (
Total abundance (a) and species richness (b) of carabid beetles in the four habitats of the alpine-subalpine zone on Mt. Hakusan.
Total carabid beetle abundance was highest on July 15, followed by July 24, and it declined thereafter (Figure
ANOSIM analyses revealed significant differences in carabid beetle compositions among the four habitats on July 15 and 24, August 13, and September 23 (significance levels < 5.0%), while marginally significant differences were evident on August 27 and September 11 (significance levels 5.0–6.6%) (Table
Global test data and pairwise statistics derived by one-way analyses of similarities (ANOSIM) that explored differences in carabid beetle assemblages among the four habitats (six sampling dates) on Mt. Hakusan. All data were fourth-root transformed prior to ANOSIM analyses.
Sampling day | Global test | Pairwise statistic | ||||||
---|---|---|---|---|---|---|---|---|
Sample statistic | Significance | SB & AM | SB & PS | SB & FF | AM & | AM & FF | PS & FF | |
July 15 | 0.764 | 0.2 | –0.250 | 1.000 | 0.815 | 1.000 | 1.000 | 0.778 |
July 24 | 0.929 | 0.1 | 0.167 | 1.000 | 1.000 | 1.000 | 1.000 | 1.000 |
August 13 | 0.564 | 0.2 | 0.667 | 0.574 | 0.944 | 0.250 | 0.917 | 0.111 |
August 27 | 0.320 | 6.6 | – | – | – | – | – | – |
September 11 | 0.333 | 5.0 | – | – | – | – | – | – |
September 23 | 0.409 | 2.2 | −0.167 | 0.519 | −0.148 | 1.000 | 1.000 | 1.000 |
Entire period | 0.849 | 0.1 | −0.250 | 1.000 | 0.852 | 1.000 | 1.000 | 0.963 |
SB, snow beds; AM, alpine meadows; PS,
Nonmetric multidimensional scaling (NMDS) ordinations based on the abundance of carabid beetles on July 15, July 24, September 23, and the entire period (pooled data) on Mt. Hakusan. Only carabid beetle species with a Pearson correlation coefficient ≥ 0.6 are shown in the graphs. Vectors indicate the species that contributed significantly to discriminate the carabid beetle assemblages among the four habitats, with long vectors indicating the species with high contributions. The 2D stress indicates the model fit.
All carabid beetle size classes were found in all habitat types (see Figure
The percentage contributions of (a) small (<10 mm), medium (10–20 mm), and large (>20 mm) carabid beetles and (b) macropterous, apterous, and brachypterous wing forms in the four habitats of the alpine-subalpine zone (altitude 2070–2600 m) and three habitats in the deciduous forest zone (altitude 140–680 m) on Mt. Hakusan. The data for the deciduous forest zone are based on Hiramatsu [
BIO-ENV analyses revealed significant associations between carabid beetle compositions and six environmental variables on July 15 and 24, August 27, and September 23 (significance levels <5%; Table
Biota-environment (BIO-ENV) analyses identifying the best five sets of environmental predictors explaining carabid beetle compositions on Mt. Hakusan.
Rank | July 15 | July 24 | August 27 | September 23 | ||||
---|---|---|---|---|---|---|---|---|
Significance level 0.1% | Significance level 0.2% | Significance level 0.2% | Significance level 2.7% | |||||
| Variable | | Variable | | Variable | | Variable | |
1 | 0.718 | Water | 0.726 | Water | 0.604 | Temperature | 0.541 | Pinus |
| ||||||||
2 | 0.680 | Water | 0.684 | Water | 0.566 | Substrate | 0.541 | Substrate |
| ||||||||
3 | 0.640 | Water | 0.679 | Water | 0.553 | Temperature | 0.534 | Water |
| ||||||||
4 | 0.621 | Water | 0.675 | Water | 0.540 | Temperature | 0.506 | Water |
| ||||||||
5 | 0.616 | Water | 0.661 | Water | 0.529 | Substrate | 0.466 | Temperature |
Water, soil water content. Substrate, substrate size. Temperature, mean ground surface temperature. Range, diurnal temperature range. Pinus, percentage coverage of
Our study showed that the carabid beetles on Mt. Hakusan could be generally classified into three distinct assemblages: those of snow beds and alpine meadows,
In addition, the carabid beetle assemblages at our study sites consisted predominantly of small species and individuals. While small carabid beetle species (<10 mm body length) constituted 52% of the total carabid beetle species in the present study, the percentage contributions of small carabid beetle species were shown to be less than 20% of the carabid beetle assemblages in lowland areas (altitude 140–680 m) including lawn, grassland, and forest at the foot of Mt. Hakusan below the current study sites [
As reported in studies of alpine carabid beetles in Europe [
Unlike the European Alps or Apennines, where the percentages of endemic carabid beetles are high [
The carabid beetle fauna in the high mountain areas of Mt. Hakusan was more similar to that of the Japanese Alps than to that at the foot of the mountain. Between 14 and 15 carabid beetle species were previously recorded in studies conducted above 2000 m altitude in the Southern and Northern Japanese Alps [
Overall, carabid beetles in the high mountain areas of Mt. Hakusan were characterized by depauperate fauna with a small number of dominant species, small body size, wingless species, and isolated populations, with some species that are commonly distributed in high mountain ecosystems of the Japanese Alps.
The total carabid beetle abundance in
By contrast, the total carabid beetle abundance fluctuated markedly in the snow beds and alpine meadows (Figure
The snow beds and alpine meadows were also characterized by high soil water content (Table
In addition to large temporal variation in the total carabid beetle abundance, intersite variation in the total carabid beetle abundance was also prominent in snow beds and alpine meadows between July 15 and 24 (Table
Although fell-fields were represented by six species of carabid beetles, only two small or medium nonmacropterous species (
Temperature also significantly affects carabid beetle compositions [
Over the past few decades, signs of global warming have been reported in mountainous areas worldwide [
In summary, the carabid beetle assemblages in the alpine-subalpine zone of Mt. Hakusan were generally characterized by small body size and reduced wings, with high habitat specificity. This study is the first to document the habitat associations and morphological traits of alpine carabid beetles on a Japanese mountain. The results conform to the general patterns reported from European mountains, which have a longer geological history and high carabid endemism [
Mountain areas are especially susceptible to global climate change [
Some of this research was a component of the Monitoring-Site 1000 Alpine Zone Survey performed by the Biodiversity Center of Japan, Ministry of the Environment.
The authors declare no conflicts of interest associated with publication of this manuscript.
The authors acknowledge Chubu Regional Environmental Office, Hakusan Ranger Office for Nature Conservation, and Shirayama Hime Shrine for allowing them to perform field surveys in the study area.
Table S1: summary of analyses of variance (ANOVA) of environmental variables among four habitats in the alpine-subalpine zone on Mt. Hakusan in central Japan. Repeated measures ANOVA was used to test differences in soil water content, ground surface temperature, diurnal temperature range, and vegetation cover among the four habitats. One-way ANOVA was used to test the difference in mean substrate size among the four habitats. Table S2: numbers of individuals (per 20 baited pitfall traps) of carabid beetles collected at 11 sites in snow beds (SB), alpine meadows (AM),