Eur. J. Entomol. 117: 430-441, 2020 | DOI: 10.14411/eje.2020.047
Feeding habits of the endangered Japanese diving beetle Hydaticus bowringii (Coleoptera: Dytiscidae) larvae in paddy fields and implications for its conservationOriginal article
- 1 Environmental Technology Division, Institute of Environmental Informatics, IDEA Consultants Inc., 2-2-2 Hayabuchi, Tsuzuki-ku, Yokohama, Kanagawa 224-0025, Japan; ORCID: https://orcid.org/0000-0002-3098-9206; e-mail: watanabe.reiya.sw@alumni.tsukuba.ac.jp
- 2 Faculty of Education, Nagasaki University, Nagasaki, Japan; e-mail: ooba@nagasaki-u.ac.jp
- 3 Graduate School of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan; e-mail: yokoi.tomoyuki.gp@u.tsukuba.ac.jp
The diving beetle Hydaticus bowringii Clark, 1864 (Coleoptera: Dytiscidae) is on the Red List of Japan as 'Near Threatened'. However, there is no quantitative information on the feeding habits of its larvae, which could be used to aid its conservation. In order to determine the prey that are important for the survival and growth of larvae of H. bowringii, we combined the results of field surveys of paddy fields and rearing experiments. In the field, H. bowringii larvae predominantly feed on tadpoles of five species of frogs and occasionally also on insects, loaches and worms. The phenology of the tadpoles was similar to that of larvae of H. bowringii, as their abundances increased from May to June and decreased in July. Experimentally reared larvae of H. bowringii grew faster when fed tadpoles than when fed Sigara nymphs or a mixture of both prey, and more emerged as adults when tadpoles were included in their diet. Adults were larger in the tadpole treatment than in the Sigara treatment. Based on these results, we conclude that tadpoles are more suitable prey for the survival and growth of larvae of H. bowringii than insects. The decline in the abundance of frogs could be one of the factors determining the decrease in the local abundances of H. bowringii. In conclusion, we affirm that in order to conserve populations of H. bowringii it is crucial to maintain paddy field environments in which frogs are abundant.
Keywords: Coleoptera, Dytiscidae, Hydaticus bowringii, diving beetle, larva, feeding, tadpole, paddy field, phenology, conservation, Japan
Received: April 19, 2020; Revised: October 6, 2020; Accepted: October 6, 2020; Published online: November 9, 2020 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Abràmoff M.D., Magalhães P.J. & Ram S.J. 2004: Image processing with imageJ. - Biophotonics Int. 11: 36-41.
- Borzée A. 2019: First amphibian behavioural observation from the Democratic People's Republic of Korea: predation of a Dryophytes japonicus tadpole by Hydaticus sp. larvae. - Nat. Conserv. Res. 4: 106-108.
Go to original source... - Brose U., Jonsson T., Berlow E.L., Warren P., Banasek-Richter C., Bersier L.F., Blanchard J.L., Brey T., Carpenter S.R., Cattin Blandenie M.-F. et al. 2006. Consumer-resource body-size relationships in natural food webs. - Ecology 87: 2411-2417.
Go to original source... - Chesson J. 1978: Measuring preference in selective predation. - Ecology 59: 211-215.
Go to original source... - Chesson J. 1983: The estimation and analysis of preference and its relationship to foraging models. -Ecology 64: 1297-1304.
Go to original source... - Cobbaert D., Bayley S.E. & Greter J.L. 2010: Effects of a top invertebrate predator (Dytiscus alaskanus; Coleoptera: Dytiscidae) on fishless pond ecosystems. - Hydrobiologia 644: 103-114.
Go to original source... - Culler L.E. & Lamp W.O. 2009: Selective predation by larval Agabus (Coleoptera: Dytiscidae) on mosquitoes: Support for conservation-based mosquito suppression in constructed wetlands. - Freshw. Biol. 54: 2003-2014.
Go to original source... - Culler L.E., Ohba S. & Crumrine P. 2014: Chapter 8: predator-prey interactions of dytiscids. In D.A. Yee (ed.): Ecology, Systematics, and the Natural History of Predaceous Diving Beetles (Coleoptera: Dytiscidae). Springer, New York, pp. 363-386.
Go to original source... - Dudová P., Boukal D.S. & Klecka J. 2019: Prey selectivity and the effect of diet on growth and development of a dragonfly, Sympetrum sanguineum. - PeerJ 7: e7881, 19 pp.
Go to original source... - Evans E.W. 1982: Timing of reproduction by predatory stinkbugs (Hemiptera: Pentatomidae): patterns and consequences for a generalist and a specialist. - Ecology 63: 147-158.
Go to original source... - Foster G.N. & Bilton D.T. 2014: Chapter 10: the conservation of predaceous diving beetles: knowns, unknowns and ancedotes. In D.A. Yee (ed.): Ecology, Systematics, and the Natural History of Predaceous Diving Beetles (Coleoptera: Dytiscidae). Springer, New York, pp. 437-462.
Go to original source... - Gould J., Valdez J.W., Clulow J. & Clulow S. 2019: Diving beetle offspring oviposited in amphibian spawn prey on the tadpoles upon hatching. - Entomol. Sci. 22: 393-397.
Go to original source... - Heinze G. & Schemper M. 2002: A solution to the problem of separation in logistic regression. - Stat. Med. 21: 2409-2419.
Go to original source... - Heinze G., Ploner M., Dunkler D. & Southworth H. 2018: Package "logistf". URL: https://cran.r-project.org/web/packages/logistf/logistf.pdf (last accessed 18 Apr. 2020).
- Ichikawa N. 2002: Declinig factors of Cybister chinensis. - Tameikenosizen 36: 9-15 [in Japanese].
- Inoda T., Hasegawa M., Kamimura S. & Hori M. 2009: Dietary program for rearing the larvae of a diving beetle, Dytiscus sharpi (Wehncke), in the laboratory (Coleoptera: Dytiscidae). - Coleopt. Bull. 63: 340-350.
Go to original source... - Japan Meteorological Agency 2020: Past Weather Data Download. URL: http://www.data.jma.go.jp/gmd/risk/obsdl/index.php#!table (last accessed 6 Jun. 2020) [in Japanese].
- Johansson A. & Nilsson A.N. 1992: Dytiscus latissimus and D. circumcinctus (Coleoptera, Dytiscidae) larvae as predators on three case-making caddis larvae. - Hydrobiologia 248: 201-213.
Go to original source... - Kawai T. & Tanida K. 2018: Aquatic Insects of Japan: Manual with Keys and Illustrations. 2nd ed. Tokai University Press, Kanagawa, 1730 pp. [in Japanese].
- Kingsley K.J. 1985: Eretes sticticus (L.) (Coleoptera: Dytiscidae): life history observations and an account of a remarkable event of synchronous emigration from a temporary desert pond. - Coleopt. Bull. 39: 7-10.
- Klecka J. & Boukal D.S. 2012: Who eats whom in a pool? A comparative study of prey selectivity by predatory aquatic insects. - PLoS ONE 7: e37741, 13 pp.
Go to original source... - Klecka J. & Boukal D.S. 2013: Foraging and vulnerability traits modify predator-prey body mass allometry: freshwater macroinvertebrates as a case study. - J. Anim. Ecol. 82: 1031-1041.
Go to original source... - Kosmidis I., Konis K., Pagui E.C.K. & Sartori N. 2020: Package 'brglm2'. URL: https://cran.r-project.org/web/packages/brglm2/brglm2.pdf (last accessed 22 Sep. 2020).
- Kurdíková V., Smolinský R. & Gvoždík L. 2011: Mothers matter too: Benefits of temperature oviposition preferences in newts. - PLoS ONE 6: e23842, 6 pp.
Go to original source... - MAFF & NARO 2012: Survey and Evaluation Manual of Biodiversity Indicators Useful for Agriculture. URL: http://www.naro.affrc.go.jp/archive/niaes/techdoc/shihyo/ (last accessed 18 Apr. 2020) [in Japanese].
- Matsui M. & Maeda N. 2018: Encyclopaedia of Japanese Frog. Bun-ichi Sogo Shuppan, Tokyo, 272 pp. [in Japanese, English abstr.].
- Ministry of the Environment of Japan 2019: Red list of Japan. URL: http://www.env.go.jp/press/files/jp/110615.pdf (last accessed 18 Apr. 2020) [in Japanese].
- Mitamura T., Hirasawa K. & Yoshii S. 2017: The Handbook of Japanese Aquatic Insect. Vol. 1: Coleoptera. Bun-ichi Sogo Shuppan, Toyo, 176 pp. [in Japanese].
- Mori M. & Kitayama A. 2002: Dytiscoidea of Japan. Bun-ichi Sogo Shuppan, Tokyo, 231 pp. [in Japanese].
- Mukai Y. 2014: Organisms Inhabiting in Rice Paddies to be Examined by Painting. Bun-ichi Sogo Shuppan, Tokyo, 80 pp. [in Japanese].
- Nakajima J., Hayashi M., Ishida K., Kitano T. & Yoshitomi H. 2020: Aquatic Coleoptera and Hemiptera of Japan. Bun-ichi Sogo Shuppan, Tokyo, 351 pp. [in Japanese].
- Nakazawa T., Ohba S. & Ushio M. 2013: Predator-prey body size relationships when predators can consume prey larger than themselves. - Biol. Lett. 9: 20121193, 5 pp.
Go to original source... - Natuhara Y. 2013: Ecosystem services by paddy fields as substitutes of natural wetlands in Japan. - Ecol. Eng. 56: 97-106.
Go to original source... - Nishida T. 2000: Habitat of Hydaticus conspersus sakishimanus larvae (II). - Gekkan-Mushi 358: 8-9 [in Japanese].
- Nishihara S. 2012: Analysis of freshwater animal community by field experiment and its application to conservation. - Jap. J. Ecol. 62: 179-186 [in Japanese, English abstr.].
Go to original source... - Nishihara S., Karube H. & Washitani I. 2006: Status and conseravtion of diving beetles inhabiting rice paddies. - Jap. J. Conserv. Ecol. 11: 143-157 [in Japanese, English abstr.].
- Nisikawa U. & Miyashita T. 2014: Social-Ecological Restoration in Paddy-Dominated Landscapes. Springer, Tokyo, 308 pp.
- Ohba S. 2009a: Feeding habits of the diving beetle larvae, Cybister brevis Aube (Coleoptera: Dytiscidae) in Japanese wetlands. - Appl. Entomol. Zool. 44: 447-453.
Go to original source... - Ohba S. 2009b: Ontogenetic dietary shift in the larvae of Cybister japonicus (Coleoptera: Dytiscidae) in Japanese rice fields. - Environ. Entomol. 38: 856-860.
Go to original source... - Ohba S. 2011: Ecological studies in lentic aquatic insects including rare species: Consideration of their conservations and applied aspects from the predator-prey relationship. - Jap. J. Environ. Entomol. Zool. 22: 39-48 [in Japanese, English abstr.].
- Ohba S. & Inatani Y. 2012: Feeding preferences of the endangered diving beetle Cybister tripunctatus orientalis Gschwendtner (Coleoptera: Dytiscidae). - Psyche 2012: 139714, 3 pp.
Go to original source... - Ohba S., Izumi Y. & Tsumuki H. 2012: Effect of loach consumption on the reproduction of giant water bug Kirkaldyia deyrolli: dietary selection, reproductive performance, and nutritional evaluation. - J. Insect Conserv. 16: 829-838.
Go to original source... - Ohba S. & Tatsuta H. 2016: Young giant water bug nymphs prefer larger prey: changes in foraging behaviour with nymphal growth in Kirkaldyia deyrolli. - Biol. J. Linn. Soc. 117: 601-606.
Go to original source... - Ohba S., Miyasaka H. & Nakasuji F. 2008a: The role of amphibian prey in the diet and growth of giant water bug nymphs in Japanese rice fields. - Popul. Ecol. 50: 9-16.
Go to original source... - Ohba S., Tatsuta H. & Nakasuji F. 2008b: Variation in the geometry of foreleg claws in sympatric giant water bug species: an adaptive trait for catching prey? - Entomol. Exp. Appl. 129: 223-227.
Go to original source... - Quintans D. 2019: Package 'electivity'. URL: https://cran.r-project.org/web/packages/electivity/electivity.pdf (last accessed 19 Sep. 2020).
- R Core Team 2019 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, URL: https://www.r-project.org/ (last accessed 18 Apr. 2020).
- Resetarits W.J. 1998: Differential vulnerability of Hyla chrysoscelis eggs and hatchlings to larval insect predators. - J. Herpetol. 32: 440-443.
Go to original source... - Ripley B., Vanables B., Bates D.M., Hornik K., Gebhardt A. & Firth D. 2020: Package 'MASS'. URL: https://cran.r-project.org/web/packages/MASS/MASS.pdf (last accessed 26 Sep. 2020).
- Saijo H. 2001: Seasonal prevalence and migration of aquatic insects in paddies and an irrigation pond in Shimane Prefecture. - Jap. J. Ecol. 51: 1-11 [in Japanese, English abstr.].
- Scholten I., van Kleef H.H., van Dijk G., Brouwer J. & Verberk W.C.E.P. 2018: Larval development, metabolism and diet are possible key factors explaining the decline of the threatened Dytiscus latissimus. - Insect Conserv. Divers. 11: 565-577.
Go to original source... - Sota T. 1985: Activity patterns, diets and interspecific interactions of coexisting spring and autumn breeding carabids: Carabus yaconinus and Leptocarabus kumagaii (Coleoptera, Carabidae). - Ecol. Entomol. 10: 315-324.
Go to original source... - Takeuchi M., Uenishi R. & Watanabe H. 2019: Habitat use of the Japanese wrinkled frog (Glandirana rugosa) within the Shonan Region, Honshu Island, Japan. - Biodiversity 20: 106-117.
Go to original source... - Taqumori R.M., Evans M.J., Soga M., Kobayashi R., Sekiya K., Miyashita T. & Yoshida K.T. 2020: Modern farming practices in paddy fields negatively affect an endemic frog, Glandirana susurra, in Japan. - Wetlands 40: 1607-1615.
Go to original source... - Tate A.W. & Hershey A.E. 2003: Selective feeding by larval dytiscids (Coleoptera: Dytiscidae) and effects of fish predation on upper littoral zone macroinvertebrate communities of arctic lakes. - Hydrobiologia 497: 13-23.
Go to original source... - Tsuzuki Y., Taniwaki A. & Inoda T. 2003: The Perfect Manuals for Breeding of Aquatic Insects. Data House, Tokyo, 255 pp. [in Japanese].
- Uruma H., Kobayashi R., Nihijima S. & Miyashita T. 2012: Effectiveness of conservation-oriented agricultural practices on amphibians inhabiting Sado Island, Japan, with a consideration of spatial structure. - Jap. J. Conserv. Ecol. 17: 155-164 [in Japanese, English abstr.].
- Walker A.A., Weirauch C., Fry B.G. & King G.F. 2016: Venoms of heteropteran insects: A treasure trove of diverse pharmacological toolkits. - Toxins (Basel) 8: 1-32.
Go to original source... - Watanabe K. 2016: The distribution of aquatic insects (Coleoptera and Hemiptera) in paddies and open ditches in rice fields in southwestern Ehime Prefecture, Japan. - Jap. J. Conserv. Ecol. 21: 227-235 [in Japanese, English abstr.].
- Watanabe K. 2017a: Relationships between endangered aquatic insects and paddy. - Nat. Insects 52: 5-8 [in Japanese].
- Watanabe R. 2017b: Field observation of hibernating individuals in Hydaticus bowringii and H. grammicus (Coleoptera: Dytiscidae). - Sayabane (New Ser.) 28: 47-48 [in Japanese].
- Watanabe R. 2019: Field observation of predation on a horsehair worm (Gordioida: Chordodidae) by a diving beetle larva Cybister brevis Aubé (Coleoptera: Dytiscidae). - Entomol. Sci. 22: 230-232.
Go to original source... - Watanabe R., Nikkeshi A. & Yokoi T. 2019: Effects of environmental factors in rice paddies and the surrounding landscape on the aquatic insect community. - Jap. J. Conserv. Ecol. 24: 49-60 [in Japanese, English abstr.].
- Wells K.D. 2007: The Ecology and Behavior of Amphibians. University of Chicago Press, Chicago and London, 1400 pp.
- Williams D.D. 2006: The Biology of Temporary Wetlands. Oxford University Press, New York, 352 pp.
- Williams F.X. 1936: Two water beetles that lay their eggs in the frothy egg masses of a frog or tree toad. - Pan-Pac. Entomol. 12: 6-7.
- Yabu S. 2005: Introduction to the Paddy Field Biotope, Comfortable Rural Environment Created by Rich Organisms. Rural Culture Association Japan, Tokyo, 159 pp. [in Japanese].
- Yee D.A., O'Regan S.M., Wohlfahrt B. & Vamosi S.M. 2013: Variation in prey-specific consumption rates and patterns of field co-occurrence for two larval predaceous diving beetles. - Hydrobiologia 718: 17-25.
Go to original source... - Zheng X. & Natuhara Y. 2020: Landscape and local correlates with two green tree-frogs, Rhacophorus (Amphibia: Rhacophoridae) in different habitats, central Japan. - Landsc. Ecol. Eng. 16: 199-206.
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.




