Open access peer-reviewed chapter
List of carabid species inhabiting different grasslands of Kakuma campus with their subfamily, tribe, abundance and ecological trait.
Abstract
Although adult feeding habits and food requirements are currently and reasonably well known for many coleopteran species, still some carabid species are with peculiar feeding guilds. Although many studies have shown a relationship between morphology of mandibles and feeding behavior in different taxal group, still many aspects concerning the feeding behavior of carabids are promising. An assemblage of carabid species was collected from Kakuma Campus grassland in Kanazawa City, Japan. These species were represented by five subfamilies and nine tribes where the highest number of tribes (3 tribes) was confined to subfamily Harpalinae. The collected carabid assemblage was subjected to mandibular analysis and being categorized into two main groups; carnivorous and omnivorous species. Homologies among mandibular characteristics and functional adaptations of the mandible were also proposed to explore how the interaction network of carabids can affect their behavior in different habitats.
Keywords
- Cleoptera
- Carabidae
- manidbles
- morpho-ecological
- feeding guild
- carnivourous
- omnivorous
1. Introduction
Coleoptera possess relatively well-known taxonomy and ecological functions, specialized habitat requirements and considered as one of the most diverse groups of insects [1, 2, 3]. It was declared that Carabidae is a megadiverse species in coleopteran family with around 33,920 valid species world-wide [3]. They are one of the dominant aboveground invertebrates in diverse pastures and natural grasslands, and possess high abundance and species diversity at soil surface [4, 5, 6], thus they are functionally important group [5, 6].
Ground beetles are known for their long legs and powerful mandibles which enable them to be voracious predators, important for the biological control of insect pests on farms [6, 7]. The adult beetles hunt primarily on the soil surface, but will occasionally climb into the foliage in search of food [7].
While many of these species’ diets are known, particularly among the Carabinae, the majority of species showed unknown feeding preference [6]. Attempts using morphological characteristics of the mandibles to investigate the feeding preference of different species of carabids have been made [6, 7, 8, 9, 10, 11, 12].
The subject of what carabids eat is not new, and numerous researchers have investigated the feeding habits and preferences of a diverse number of carabids [6, 12]. Their studies have offered information on the feeding habits and carabids’ feeding preferences [12].
The current study tries to find an answer for the original question: do mandibular morphological characters of adult carabid beetles could give a prediction on their feeding preferences?
Based upon feeding observations by Forbes, as probably the first to examine and describe the mandibles of carabids, who surmised that carabids were herbivorous as well as carnivorous [13]. Other researchers have supported these observations and well establishing carnivory, granivory and herbivory feeding behavior by carabids [14, 15, 16, 17, 18, 19, 20, 21, 22]. However, many carabid species may have seasonal diets, being carnivorous during part of the year and largely granivorous or herbivorous at other times [20].
In general, carabid mandibles are mostly similar [23], they were described as “three sided pyramids” and Jeannel [23] was one of the first who developed the nomenclature for the teeth and ridges (Figure 1). Indeed, the terminology was then reviewed and expanded by Acorn and Ball [10]. They described the array of teeth and elevations observed on the mesial margins of the mandibles as a series of parallel ridges separated by occlusal grooves. The terebral ridges posterior to the incisors shear; the retinacular teeth and ridges, may also shear, or, act as a compacter [10]. The variable basal region may have one or more teeth or ridges for additional reduction of food, or have a flattened basal face. A basal face may or may not support a basal brush. The basal brush of hairs may be extensive, or, confined to a few hairs, that help transfer the food to enter the mouth through the pharynx. Generally in the current study, based on personal observations, the left mandible was comparatively the dominant mandible being longer and sliding over the dorsal side of the right mandible, although, within the species, there were some observed exceptions (Figure 2).
Figure 1.
Diagram of the right mandible of a carabid beetle model showing the main parts: a: Incisor width, b: Mandibular length (l), c: Mandibular base width (w), d: Incisor area, e: Molar area, f: Mandibular width, g: Abductor muscle attachment to the mandible, h: Molar width showing grooves inside the mandible, i: Incisor.
Figure 2.
Difference in mandibular characteristics between predatory carabid (A) represented by
Based on collaborative work, we investigated the ecological traits and specifically the feeding guilds of carabid beetles (Coleoptera: Carabidae) in the grasslands ecosystem located in Kakuma Campus within Kanazawa University, Kanazawa City, Ishikawa prefecture, Japan.
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2. Materials and methods
2.1 Study area
The survey of carabid assemblage was conducted in Kakuma Campus grassland - 36.546 N & 136.708 E - within Satoyama area of Kanazawa City, Ishikawa Prefecture, Japan. Kanazawa city is located on the area facing Japan Sea being boarded by the Japan Alps, Hakusan National park and Noto Peninsula National Park. Kanazawa city sits between two rivers - Sai and Asano Rivers - covering an area of ca. 467.77 km2. Satoyama, as a part of Kanazawa; covers an area of ca. 74 ha and is located at 150 m altitude, 5 km southeast from the city center. The area comprises various habitat types ranging from secondary forests dominated by
2.2 Sampling protocol
Specimens were collected primarily from unbaited pitfall traps. At the sampling site, 15 unbaited pitfall traps were installed as trapping tools and spaced about 1 m apart along a transect running north to south through the center of each survey site. The total number of traps in all sampling habitats was 75. In most excursions, sampling of carabids was performed during the days in the middle of the month especially sunny days. Traps were installed in the soil to cover the period from early May till late November, 2019.
The traps consisted of white polyethylene beakers (13.5 cm deep, Ø 9 cm). These beakers were primed with 10% ethylene glycol and we added few drops of ordinary detergent to reduce surface tension. Three wooden sticks were drilled around each pitfall trap (11 cm below the upper brim) and a plastic beaker cover was mounted above each trap to prevent flooding by frequent rainfall and to minimize the damage that could be caused to the traps by the falling leaves or small twigs. The disturbance caused by placing the pitfall traps was minimized and the vegetation around the traps was kept intact. The ‘digging in’ effect was thus considered negligible and the traps were set immediately [6, 24, 25]. Traps were left open for two consecutive days and in the third day; each trap was emptied from its content and the specimens caught were preserved in Renner’s solution (40% ethanol, 30% water, 20% glycerin, 10% acetic acid) [26]. Preserved specimens were then brought back to the laboratory for identification, counting and sorting. To reduce the variability caused by sampling error, only one of the authors (W.M.E.) was responsible for making counts in this study.
2.3 Identification and nomenclature
Carabids were identified to species level and the used nomenclature was in accordance with the key given by Nakane [27]. In addition, the collected species were compared with already identified museum specimens in Kanazawa University for further confirmation. Collected specimens of carabids were deposited and cataloged in Kanazawa University repository room. These specimens were kept in special boxes containing small sachets enclosing naphthalene-coated tablets for further specimen protection against moths and other destructive pests. These sachets were checked regularly and renewed whenever needed.
2.4 Abundance code
Carabid species were categorized into three abundance codes according to the cumulative number of collected specimens during the study period. These abundance code are: Rare ≤5, O: 5 < Occasional ≤15 and A: Abundant >16 individuals.
2.5 Body size
Morphometric measurements of collected carabid species using Vernier® caliper micrometer (precision ±0.10 cm) were performed. Measurements were performed from the tip of the labrum to the extremity of the pygidium and carabids were classified into three body size groups: small (≤ 5 mm), medium (5 mm < body length < 15 mm) and large species (≥15 mm).
2.6 Mandibular analysis and characteristics
All specimens were dissected retaining the head capsule possessing the attaching mandibles. The head capsules were mounted on double-sided tape on slides trays. The head capsules were then precisely dissected retaining the mandibles for further analysis and to take images. Mandibles were lightly brushed with 80% ethanol then by distilled water in an effort to remove most of the soil particles and debris adhered to the mandibles. After air-drying, specimens were examined under Stereo-fluorescence microscope (Nikon® SMZ800 series) equipped with digital camera and TFT LCD Nikon® monitor where illumination was provided from double gooseneck illuminator (Olympus® HLL-301). Syncroscopy Auto-Montage system was taken for photography (Kanazawa University, Laboratory of Biodiversity). All mandibular images were saved and stored as jpeg files for morphological measurements using Image J 1.45 software.
The mandibles were identified morphologically as left and right mandibles when viewed dorsally with the head forwarded to the top of the examining slide. The main measurements were taken of both mandibles: length (l) and width (w) and compared as ratios (l/w). Measurements were performed in millimeter (mm). Mandibular length was considered from the exterior edge of the dorsal mandibular condyle to the farthest point of the mandibular incisor. On the other hand, the mandibular width was measured from the exterior edge of the dorsal mandibular condyle to the point where attachment for the abductor muscle could be observed (Figure 1).
2.7 Feeding guild
From the structure and morphological adaptations of the mandibles, two guilds were mainly assigned: predators (sharp incisors and long terebral ridge) and omnivorous species (dull incisors with short terebral ridge) [6]. Our analyses of mandibular morphology were compared with previous literature whenever data are available.
The feeding guild was predicted from mandibular morphology (Figure 1) and compared with previous reports whenever information were available.
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3. Results
3.1 Carabid assemblage
A total of 120 individuals of different carabid species belonging to 17 species were recorded from Kakuma Campus grassland. These individuals belonged to five subfamilies and eight tribes (Table 1). Subfamily Harpalinae proved to possess the highest number of tribes (3 tribes: Anisodactylini, Harpalini and Zabrini) compared to other observed subfamily in the study area. On the other hand, two subfamilies (Carabinae and Zabrinae) harbored only a single tribe each (Carabini and Callistini, respectively). Subfamily Pterostichinae proved to harbor the highest number of individuals (69 carabid individuals) and this was followed by subfamily Zabrinae (33 individuals). The least number of carabids (2 individuals) was confined to Subfamily Bembidiinae. The highest number of species in one tribe was observed in Callistini (4 species) (Table 1).
| Taxa | Individual | Ecological traits* | ||
|---|---|---|---|---|
| I | II | III | ||
| 1 1 | R R | S S | Omn Omn | |
| 3 10 3 1 | R O R R | M M M S | Omn Omn Omn Omn | |
| 6 3 | O R | L L | Car Car | |
| 19 13 11 16 10 | A O O A O | M M M L M | Car Car Car Car Car | |
| 5 7 6 5 | R O O R | L M M L | Car Car Car Car | |
Table 1.
Ecological trait:
[R: Rare ≤5, O: 5 < Occasional ≤15, A: Abundant >16].
In general, Kakuma Campus grassland revealed that the study site relatively possessed poor carabid assemblage. According to the cumulative number of individuals of each carabid species; the assemblage showed that rare species were the dominant code where this code comprised ca. 47.1% of the assemblage (Table 1). On contrary, the Abundant code (A) comprised ca. 11.76% of carabids co-occurring in Kakuma Campus grassland (Table 1).
3.2 Body size
There was a large difference between the number of carabid species with medium-sized bodies and those of other sizes. The majority of carabid species had a medium-sized body. There were 9 medium-size carabids out of 17 species, representing ca. 53% of the total observed species. Large and small-sized species were rare (only 3 species, representing ca. 17.6% of the total observed species) as indicated in Table 1. Thus, generally on the habitat level, grassland in Kakuma Campus showed a predominance of species with a medium body size (Table 1). On the other hand, on the subfamily level, medium-size carabids were distributed among three subfamilies (Harpalinae, Pterostichinae and Zabrinae) as indicated in Table 1. It was observed that small-size carabids were rare in term of number of individuals and were distributed in only two subfamilies (Subfamily Bembidiinae and Harpalinae) and it was apparent that the small-size carabids were singleton species (Table 1). On the other hand, the number of large-size carabids fell in the middle of this continuum with five large-size species could be observed and distributed in three subfamilies (Table 1) representing almost the third of the total catch (29.4%, Table 1).
3.3 Feeding guild
Out of the 17 recorded sampled species; 11 species (64.7%) were carnivorous species while only 6 species (35.3%) were omnivorous (Table 1). Most of the carnivorous were belonging to three subfamilies (Carabinae, Pterostichinae, and Zabrinae) with the maximum number of species (5 species) belong to subfamily Pterostichinae. On the other hand, omnivorous species were confined to only two subfamilies (Bembiidinae and Harpalinae) with the highest number of omnivorous species were recorded in subfamily Harpalinae (Table 1). In general, 19 individuals of carabid were observed to be omnivorous, whereas the carnivorous feeding habit was possessed by 101 carabid individuals.
Typical carnivorous species were characterized by forward-projecting mandibles, sharp incisors used to pierce and capture prey and a long terebral ridge used to kill and slice prey into pieces (Figure 2). Omnivorous species, on the other hand, had a wide molar region for crushing seeds but incisors were blunt and the terebral ridge was short as the shown example,
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4. Discussion
The Carabidae is considered one of the six largest families in the order Coleoptera and largest family in the suborder Adephaga, with ca. 33,920 valid species world-wide [3]. Some studies estimated that there are 30,000 specie [28] while other studies estimated that the number of carabid species may reach 40,000 species in the world [29]. Carabids have been extensively collected and studied because they exist in a wide range of habitats and can be relatively abundant, and are often agriculturally pertinent [1, 6]. In the present research, however, Kakuma Campus grassland showed a relatively poor assemblage of carabid species. Similar studies, declared that in one-year studies 20–35 species are found in the qualitative structure of ground beetles of cultivation fields in Central Europe Basedow et al. (1976) and Thiele (1977) [30, 31]. Moreover, in the Subcarpathian region, 54 Carabidae species were recorded with the average number of carabids species per site was 15 species [32], and the review publication reported a relatively low number of carabid species in which 12 12 species were recorded in one site out of 21 identified species in total studied sites [32].
Kakuma Campus grassland, as a part of Satoyama, was subjected to relatively low anthropogenic disturbances over a considerable time. These disturbances were focused mainly on regular monthly mowing. Prior excursions in the selected site revealed that the area is relatively with poor carabid diversity parameters compared to other sites within Satoyama, for example Kitadan area within Satoyama landscape [6]. However, more data are required to clarify more aspects concerning carabid assemblage (some of the data on other sites concerning this project were not published yet for comparisons).
Diverse studies showed that there is a long history of success in using carabids to signal environmental change [4, 8, 33, 34, 35]. Moreover, changes in landscape such as fragmentation [36, 37], recreational use [38], urbanization [39, 40], forest management [35, 41].
We assume that poor carabid assemblage as being represented by dominant rare species and relatively scarcity of abundant species in Kakuma Campus grassland as a result of regular mowing which led to relatively poor assemblage [42]. This view could be supported by other related studies which suggested that carabids could been used as indicators of large-scale environmental changes [43], and predictors of future landscape changes [4, 44].
Moreover, worth noting that fragmentation of continuous habitats, as the case of Satoyama, into many small patches or relatively small habitats as a result of anthropogenic impact such as urbanization and/or cultivation may affect the co-occurring carabids making some populations highly isolated [4, 45, 46].
In the present study, carabid species possessed diverse morphological traits which were focused mainly on body size and mandibular characteristics. There were numerous investigations dealing with morphological traits of carabids and their life strategies among different habitats [47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57].
The co-occurring carabids were predominated by small and medium-size species and large-size species were the least dominant. Other studies support our findings in which they suggested that large-bodied carabids were missing from many small islands and generally less abundant when present, with the opposite true for smaller-bodied species (Bell et al. 2017). Similar findings have been reported for carabids in relation to size of forest patches [10, 44].
Nonetheless, some studies stated that the prevailing tendency towards a relatively higher number of both small~medium size carabids is a typical phenomenon, characteristic of habitats that are subjected to external factors [58, 59].
Feeding guild was an additional important trait used to analyze the structure of carabidofauna [6, 32]. The collected carabids were dominated by carnivorous species. A similar study revealed that zoophages (predators or carnivours in other terms) were predominant in the entire assemblage [32].
Diverse studies ranked carabids into three main categories according to their pattern of food intake: oligophagous predators, polyphagous predators and phytophages. Granivory habit was, consequently, confirmed by a wide-range of diverse studies [8, 9, 10, 16, 17, 18, 22, 29, 30, 60, 61, 62, 63, 64, 65, 66]. Other studies stated that enormous number of carabid individuals may exist in farm fields, in communities of carnivore and granivores and, more in deed, obligate omnivore guilds [67].
Typical carnivorous species were characterized by forward-projecting mandibles, sharp incisors used to capture and pierce the prey. The mandible was with a long terebral ridge used to kill and slice prey into pieces. Diverse studies showed that the diet of carabids included Collembola, earthworms, nematodes, slugs, snails, aphids, eggs and larvae of Diptera and Coleoptera, Lepidoptera pupae and seeds of herbaceous plants [2, 20, 68, 69]. Hence, carabids are crucial predators in agricultural landscapes feeding on a wide-range of preys [70].
Beetles use their mandibles for prey capture and the forces created by the mandible tips are used to hold prey and pierce the integument [71, 72].
Omnivorous species, on the other hand, had a wide molar region for crushing seeds but incisors were blunt and the terebral ridge was short [6]. Thus, omnivorous species have features that are advantageous for seed feeding but reduce the efficiency of feeding on prey [6, 12].
Although adult feeding habits and food requirements are currently and reasonably well known for many carabid species, still some carabid species with peculiar feeding guilds. Some morpho-functional studies have shown a relationship between morphology and feeding behavior in the larval stage [73]. Some morpho-ecological types were defined in the European temperate zone and places most Harpaline and Zabrine, especially the larval stage, with a phytophagous diet pattern into the morpho-ecological types [73]. Nevertheless, these types were minimized into two simpler main categories: a – spermophagous (seed predators); b – c-shaped harpalines, excluding the subtribe Ditomina [74].
Ultimately, the apparent similarities between these mandibles and the jaws of various mammals are remarkable to consider [10, 31]. The incisor area of the mandibles of beetles is related to the cutting incisors encountered in rodents and lagomorphs. The posterior molars of most mammals, on the other hand, are geared to adapt the function of grinding function requiring cusps occluding into basins. This does not appear to be the case in the carabids reviewed here (based on personal observations).
The study of mandibular traits in carabids is obvious to be of significant interest, since they may be beneficial in systematic research and can be linked to feeding patterns employing simple functional explanations [6].
The gathered data on the comparatively small sample of surveyed carabid taxa give only a hint concerning the whole story of evolution of mandibular morpho-functional characteristics in adult carabids.
We hope that other studies will find the morpho-functional studies of carabid mandibles.
It is hoped that more researchers will find the study of mandibles is rewarding and will contribute to the advancement of our knowledge. The study offered here opens the door for more studies to analyze more mandibles from more carabid taxa. We believe that carabidologists would benefit greatly from these studies in their efforts to understand the evolution and adaptations of carabid beetle taxa.
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5. Conclusion
In conclusion, further studies would benefit from the examination of additional carabid taxa since making a general connection between mandibular morphological dentition and dietary pattern - generally feeding guild- is far from precise evaluation. Other evolutionary relative lineages among Carabidae are required in order to better address their precise feeding guilds. From that view, incorporation of mandibular morpho-ecological features studies together with phylogenetic analysis are recommended. Consequently, further examination of the gut contents of carabid taxa in conjunction with laboratory investigations and precise observations of feeding behavior in diverse habitats could be employed as confirmation cues for not placing carabids in an ambiguous feeding guild. To summarize, studies merely on morphological characteristics of carabid mandibles are difficult to interpret without an understanding of the functional consequences of variations in mandibular configurations in different carabids habitats. This would reveal some hidden aspects that could not be deduced from the morphological characters of the mandibles if they were adopted alone.
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Acknowledgments
The authors wish to acknowledge the staff at the Laboratory of Ecology, Graduate School of Natural Science and Technology, Kanazawa University for their sincere assistance and prompt provided facilities. Also, sincere and warm gratitude is extended to Prof. Dr. Nakamura Koji (Kanazawa University, Japan) for his keen and endless hospitality and encourages for completing the research and writing the manuscript.
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Conflict of interest
The authors declare that there are no conflict of interest associated with this article.
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