Research Article |
Corresponding author: Masakazu Hayashi ( hgf-haya@green-f.or.jp ) Corresponding author: Shinji Sugiura ( sugiura.shinji@gmail.com ) Academic editor: John Spence
© 2021 Masakazu Hayashi, Shinji Sugiura.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hayashi M, Sugiura S (2021) Shell-breaking predation on gastropods by Badister pictus (Coleoptera, Carabidae) with strikingly asymmetric mandibles. In: Spence J, Casale A, Assmann T, Liebherr JК, Penev L (Eds) Systematic Zoology and Biodiversity Science: A tribute to Terry Erwin (1940-2020). ZooKeys 1044: 815-830. https://doi.org/10.3897/zookeys.1044.62293
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The adults and larvae of some groups in the coleopteran family Carabidae are known to prey on snails (Mollusca: Gastropoda). Most species of the carabid tribe Licinini are believed to feed on live snails. However, the snail-eating behavior of only a few species has been studied. Whether adults of the licinine genus Badister can prey on live snails was tested by providing 155 live snails of 20 species (eleven terrestrial and nine aquatic species) to adults of Badister pictus Bates, 1873, and observing their behavior under laboratory conditions. Six of the 20 snail species have an operculum that can close the aperture of the shell. Each B. pictus adult attacked all of the snails provided. Badister pictus successfully preyed on ten terrestrial and six aquatic snail species. These beetles used their strikingly asymmetrical mandibles to break the dextral shells along the dorsal part of the whorls from the outer lip of the aperture towards the apex, allowing subsequent consumption of the soft bodies. However, 41.9% of snails could not be eaten by B. pictus adults. The rate of predation success by B. pictus decreased with increasing shell size and thickness of snails. In addition, the presence of an operculum decreased the rate of predation success by B. pictus. The results show that the shell size, thickness, and operculum of some snail species could play important roles in preventing B. pictus mandibles from breaking the shells. Therefore, Badister beetles may exert selective pressure on the evolution of defensive shell structures in small-sized snails.
Anti-predator defense, Badister, freshwater snail, Gastropoda, land snail, Licinini
Gastropods protect their soft bodies from predators through shells (
In the coleopteran family Carabidae, adults and larvae of some groups are snail hunters (
The licinine genus Badister Clairville, 1806, which comprises 48 species, is found in all zoogeographical regions (
Badister pictus is found in the wet grasslands along paddy fields, lakeshores, and riverbanks of Japan, Taiwan, and Russia (
The specimens of B. pictus and snail shells (except broken shells) examined in this study were deposited at the Hoshizaki Institute for Wildlife Protection (HOWP), Izumo, Japan.
Gastropod species and predation by Badister pictus observed in this study.
Family | Species | Habitat* | Eaten by beetles | Shell size and shape | |||||
---|---|---|---|---|---|---|---|---|---|
% | N | Stage† | Size‡ | H/W§ | Chirality | Operculum | |||
Achatinidae | Opeas pyrgula Schmacker & Boettger, 1891 | Ter | 91.7 | 12 | J, A | 2.4–7.7 | 2.0–3.4 | Dextral | Absent |
Alycaeidae | Metalycaeus hirasei (Pilsbry, 1900) | Ter | 0.0 | 10 | A | 3.8–4.3 | 0.6–0.7 | Dextral | Present |
Assimineidae | Assiminea japonica Martens, 1877 | Aqu | 0.0 | 4 | J | 5.0–5.4 | 1.1–1.5 | Dextral | Present |
Camaenidae | Aegista aemula (Gude, 1900) | Ter | 100.0 | 1 | J | 6.5 | 0.6 | Dextral | Absent |
Euhadra dixoni (Pilsbry, 1900) | Ter | 33.3 | 3 | J | 6.4–8.4 | 0.7–0.8 | Dextral | Absent | |
Euhadra idzumonis (Pilsbry & Gulock, 1900) | Ter | 100.0 | 11 | J | 3.1–3.9 | 0.6–0.8 | Dextral | Absent | |
Euhadra subnimbosa (Kobelt, 1894) | Ter | 100.0 | 1 | J | 5.6 | 0.8 | Dextral | Absent | |
Cyclophoridae | Cyclophorus herklotsi Martens, 1860 | Ter | 22.2 | 9 | J | 4.2–7.0 | 0.8–1.0 | Dextral | Present |
Diplommatinidae | Diplommatina sp. | Ter | 20.0 | 10 | J, A | 3.1–4.5 | 1.7–2.0 | Dextral | Absent |
Euconulidae | Yamatochlamys sp. | Ter | 100.0 | 1 | A | 3.7 | 0.6 | Dextral | Absent |
Gastrodontidae | Zonitoides arboreus (Say, 1816) | Ter | 100.0 | 14 | J, A | 2.8–4.4 | 0.4–0.6 | Dextral | Absent |
Lymnaeidae | Pseudosuccinea columella (Say, 1817) | Aqu | 58.8 | 17 | J, A | 5.9–12.5 | 1.6–1.8 | Dextral | Absent |
Physidae | Physa acuta Draparnaud, 1805 | Aqu | 80.0 | 15 | J, A | 3.8–8.1 | 1.6–1.9 | Sinistral | Absent |
Planorbidae | Gyraulus tokyoensis (Mori, 1938) | Aqu | 100.0 | 1 | A | 3.9 | 0.2 | Dextral | Absent |
Hippeutis cantori (Benson, 1850) | Aqu | 100.0 | 15 | J, A | 3.8–7.7 | 0.2–0.4 | Dextral | Absent | |
Polypylis hemisphaerula (Benson, 1842) | Aqu | 100.0 | 2 | A | 4.4–4.9 | 0.3–0.5 | Dextral | Absent | |
Semisulcospiridae | Semisulcospira libertina (Gould, 1859) | Aqu | 40.0 | 10 | J | 5.0–7.0 | 1.5–2.0 | Dextral | Present |
Stenothyridae | Stenothyra japonica Kuroda, 1962 | Aqu | 0.0 | 12 | A | 4.1–4.7 | 1.5–1.9 | Dextral | Present |
Diapheridae | Sinoennea iwakawa (Pilsbry, 1900) | Ter | 66.7 | 3 | A | 3.1–3.2 | 1.8–1.9 | Dextral | Absent |
Viviparidae | Sinotaia quadrata histrica (Gould, 1859) | Aqu | 0.0 | 4 | J | 6.2–6.3 | 1.1–1.1 | Dextral | Present |
A stereomicroscope (SMZ-1000, Nikon, Tokyo, Japan) with a CCD camera unit (Digital Sight, DS-L2, Nikon, Tokyo, Japan) and a scanning electron microscope (JCM-6000 Neoscope; JEOL Ltd., Tokyo, Japan) were used to observe and photograph the mandibles of B. pictus. The photographs taken using the stereomicroscope were stacked using Adobe Photoshop CS2 for Macintosh. The samples used for scanning electron microscope (SEM) observations were dehydrated and gold-coated using high-vacuum evaporation (Smart Coater, DII-2910SCTR, JEOL Ltd., Tokyo, Japan). The morphology of the mandibles, especially the asymmetry of the left and right mandibles, was investigated. The terminology for mandibular morphology follows
Adults of B. pictus were individually placed in plastic containers (size W 129 × D 99 × H 60 mm, capacity 500 mL) with wet paper (Kimwipe S-200: Nippon Paper Crecia Co. Ltd., Tokyo) under laboratory conditions (mean temperature, 29.1 °C; range: 25–31 °C) between 25 July and 2 September 2020. The feeding behavior of each B. pictus adult was observed by the unaided eye in a well-lit laboratory during the daytime, as described below.
A live snail was placed within the field of view of a single B. pictus in its plastic container. Terrestrial and aquatic snails were provided to B. pictus under the same conditions. When the B. pictus adult attacked the snail, feeding behavior was observed. If the B. pictus adult could not successfully prey on the snail, another snail was provided. However, no B. pictus adult was fed more than one snail per day. Beetles were starved for 22–29 h before the feeding experiments. Snails with soft bodies that were not injured were considered to have survived, even if the shell or operculum were partially damaged. Adults of B. pictus were repeatedly used in feeding experiments (mean ± SE 14.1 ± 4.8 snails exposed per adult beetle), although individual snails were used only once. The raw data are available from the Figshare Digital Repository (https://figshare.com/s/89fdf111feea86bb8626).
Shell morphological characteristics, such as shell size and thickness, were examined to clarify how these factors affected the ability of B. pictus adults to open them. The sizes of the shells were measured from the images taken using a Canon Eos70D (Canon Inc., Tokyo, Japan) with a macro lens (MP-E 65 mm; Canon Inc., Tokyo, Japan) at equal magnification. Each image was magnified 115 times and measured using the digital image processing software Preview ver. 10.1 (Apple Inc.). The maximum height and width of the shells were measured to the closest 0.1 mm. The aperture thickness of some shells (63 shells of 14 species) was also measured (Fig.
Generalized linear mixed models (GLMMs) with a binomial error distribution and a logit link were used to elucidate the factors affecting successful predation of snails (R software version 2.15.3 with the lme4 package 0.999999-0;
Similar to other Badister species, B. pictus had clearly asymmetric mandibles (Fig.
Mandibles of adult Badister pictus A, B photos from a stereoscopic microscope C–I photos by a SEM A, C dorsal view B, D dorsal view (from the front) E dorsal view (from the left mandible) F dorsal view (from the right mandible) G lateral view (from the left mandible) H lateral view (from the right mandible) I dorsal view of closed mandibles (from the right mandible). “d” indicates a depression of the left mandible; “n” indicates a dorsal notch of the right mandible; “tt” indicates a terebral tooth of the right mandible. All antennal segments (except the first segment) and all setae on labrum were removed in C–H.
All adults of B. pictus always attacked the provided snails. Of the 75 terrestrial snails (11 species), 61.3% (10 species) were eaten by B. pictus, whereas 55.0% of 80 aquatic snails (six of nine species) were eaten (Table
Beetle adults always began their attacks by breaking the outer lip of the dextral (right-coiled) shells (Figs
Attacking and feeding behavior of Badister pictus adults A adult biting the outer lip of Zonitoides arboreus (Say, 1816) B adult feeding on the soft body after opening the shell of Z. arboreus C adult breaking the shell of Opeas pyrgula Schmacker & Boettger, 1891 D adult biting the outer lip of Metalycaeus hirasei (Pilsbry, 1900) E adult feeding on the soft body from the broken shell of Hippeutis cantori (Benson, 1850) F adult biting the basal lip of the sinistral snail Physa acuta Draparnaud, 1805.
Shells broken by Badister pictus A Cyclophorus herklotsi Martens, 1860 B Diplommatina sp. C Semisulcospira libertina (Gould, 1859) D, E Physa acuta F Gyraulus tokyoensis (Mori, 1938) G Hippeutis cantori H Polypylis hemisphaerula (Benson, 1842) I Pseudosuccinea columella (Say, 1817) J Opeas pyrgula K Zonitoides arboreus L Sinoennea iwakawa (Pilsbry, 1900) M Aegista aemula (Gude, 1900) N, O Euhadra idzumonis (Pilsbry & Gulock, 1900) P adult B. pictus A, F, G, H, K, M, N dorsal view B, C, D, J, L, O front view E, I back view. The soft bodies of these snails were eaten by B. pictus.
Shell morphology and bite traces of Badister pictus A dextral shell B sinistral shell C dextral shell with an operculum D–F bite traces on dextral shells G, H bite traces on sinistral shells I broken part (shaded area) on a sinistral shell A–D, G front view E, H, I back view F dorsal view. Red circles indicate the positions where the shell (aperture) thickness was measured. Red arrows indicate the starting point of shell breaking by B. pictus. Broken lines indicate the bite traces by B. pictus.
Shells of snails surviving attack by Badister pictus A, B Cyclophorus herklotsi C, D Metalycaeus hirasei E Diplommatina sp., 1904 F, G Sinotaia quadrata histrica (Gould, 1859) H, I Assiminea japonica Martens, 1877 J Stenothyra japonica Kuroda, 1962 K, L Semisulcospira libertina M Physa acuta N Pseudosuccinea columella O adult B. pictus attacking Diplommatina sp. A, C, F dorsal view B, D, E, G, H, J, K, N front view I, L, M back view. The soft bodies were not eaten by B. pictus, although some shells were partially broken.
The rate of successful predation on snails by B. pictus decreased with increasing shell size (Fig.
Feeding on sinistral (left-coiled) snails (Physa acuta Draparnaud, 1805) by B. pictus was also observed. All juveniles (N = 12) of P. acuta were eaten by B. pictus, whereas all adults (N = 3) of P. acuta survived the attack. Badister pictus adults started breaking the basal lip (i.e., the opposite side of the outer lip) or the shell wall from the exterior side of the body whorl of P. acuta (Figs
Effects of shell size/thickness and operculum on predation success of Badister pictus A relationship between maximum shell height/width and the presence/absence of an operculum and predation success (N = 155) B relationship between the shell thickness and the presence of an operculum and the predation success (N = 55). Red triangles and blue circles show snails with and without an operculum, respectively. Red and blue lines represent logistic regression lines of snails with and without an operculum derived from generalized linear mixed models, respectively (Tables
Results of a generalized linear mixed model investigating the effects of shell size and operculum presence on predation by Badister pictus.
Response variable | Explanatory variable | Coefficient estimate | SE | z value | P value |
---|---|---|---|---|---|
(fixed effect) | |||||
Predation success | Intercept | 11.986 | 2.603 | 4.605 | 0.000004 |
Shell size | –1.559 | 0.377 | –4.135 | 0.000036 | |
Operculum presence* | –8.725 | 2.477 | –3.523 | 0.000427 |
Results of a generalized linear mixed model investigating the effects of shell thickness and operculum presence on predation by Badister pictus.
Response variable | Explanatory variable | Coefficient estimate | SE | z value | P value |
---|---|---|---|---|---|
(fixed effect) | |||||
Predation success | Intercept | 9.1669 | 3.0543 | 3.001 | 0.00269 |
Shell thickness | –0.1079 | 0.0446 | –2.418 | 0.01559 | |
Operculum presence* | –2.9508 | 2.6212 | –1.126 | 0.26028 |
Most species of the tribe Licinini are believed to be snail hunters (
Badister pictus is found in wet grasslands, such as paddy fields, in Japan (
The mandibles and snail-eating behavior of B. pictus observed in this study were similar to those of Licinus adults reported in a previous study (
As most terrestrial snails have dextral shells, licinine beetles most often encounter right-coiled prey.
Diverse shell morphologies of gastropods have been discussed in terms of anti-predator defenses (
We are grateful to K. Mashino and K. Kawano for their assistance with identifying the terrestrial and aquatic gastropod species. We thank H. Kamezawa for providing information regarding the references. We also thank the editor and reviewers for their helpful comments on an earlier version of the manuscript.
Movie 1. Badister pictus attacking a dextral snail Zonitoides arboreus.
Data type: images
Explanation note: Beetle adults always started breaking the outer lip of the dextral (right-coiling) shells.
Table S1. Results of a generalized linear mixed model for effects of shell size, operculum presence, and the interaction on predation by Badister pictus.
Data type: Table
Explanation note: Results of a generalized linear mixed model.