Which Seed Properties Determine the Preferences of Carabid Beetle Seed Predators?
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Seed Material
2.2. Preference Experiments
2.3. Measurement of Seed Morphological Traits
2.4. Chemical Analysis of Seeds
2.5. Ecology and Taxonomy of Plants
2.6. Data Analyses
3. Results
3.1. Preferences of Carabids
3.2. Morphological Analysis of Seeds
3.3. Chemical Analyses of Seeds
3.4. Relationships among Carabid Preferences and Seed Properties
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Thiele, H.U. Carabid Beetles in Their Environments; Springer Science & Business Media: Berlin, Germany, 1977. [Google Scholar]
- Hůrka, K. Carabidae of the Czech and Slovak Republics. Carabidae České a Slovenské Republiky; Kabourek: Zlín, Czech Republic, 1996; p. 565. [Google Scholar]
- Frei, B.; Guenay, Y.; Bohan, D.A.; Traugott, M.; Wallinger, C. Molecular analysis indicates high levels of carabid weed seed consumption in cereal fields across Central Europe. J. Pest Sci. 2019, 92, 935–942. [Google Scholar] [CrossRef] [Green Version]
- Lundgren, J.G.; Saska, P.; Honek, A. Molecular approach to describing a seed-based food web: The post-dispersal granivore community of an invasive plant. Ecol. Evol. 2013, 3, 1642–1652. [Google Scholar] [CrossRef] [PubMed]
- Lundgren, J.G.; Rosentrater, K.A. The strength of seeds and their destruction by granivorous insects. Arthropod-Plant Interact. 2007, 1, 93–99. [Google Scholar] [CrossRef]
- Honek, A.; Martinkova, Z.; Saska, P.; Pekar, S. Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera). Basic Appl. Ecol. 2007, 8, 343–353. [Google Scholar] [CrossRef]
- Saska, P.; Honek, A.; Martinkova, Z. Preferences of carabid beetles (Coleoptera: Carabidae) for herbaceous seeds. Acta Zool. Acad. Sci. Hung. 2019, 65, 57–76. [Google Scholar] [CrossRef]
- Forsythe, T.G. Feeding Mechanisms of Certain Ground Beetles (Coleoptera: Carabidae). Coleopt. Bull. 1982, 36, 26–73. [Google Scholar]
- Honek, A.; Saska, P.; Martinkova, Z. Seasonal variation in seed predation by adult carabid beetles. Entomol. Exp. Appl. 2006, 118, 157–162. [Google Scholar] [CrossRef]
- Dalling, J.W.; Davis, A.S.; Schutte, B.J.; Arnold, A.E. Seed survival in soil: Interacting effects of predation, dormancy and the soil microbial community. J. Ecol. 2011, 99, 89–95. [Google Scholar] [CrossRef]
- Mazer, S.J. Rainforest plants protect their investments. Trends Ecol. Evol. 1998, 13, 471–473. [Google Scholar] [CrossRef] [PubMed]
- Saska, P.; Foffová, H.; Martinková, Z.; Honěk, A. Persistence and Changes in Morphological Traits of Herbaceous Seeds Due to Burial in Soil. Agronomy 2020, 10, 448. [Google Scholar]
- Maureaud, A.; Andersen, K.H.; Zhang, L.; Lindegren, M. Trait-based food web model reveals the underlying mechanisms of biodiversity-ecosystem functioning relationships. J. Anim. Ecol. 2020, 89, 1497–1510. [Google Scholar] [CrossRef] [PubMed]
- Zaguri, M.; Hawlena, D. Odours of non-predatory species help prey moderate their risk assessment. Funct. Ecol. 2020, 34, 830–839. [Google Scholar] [CrossRef]
- Antiqueira, P.A.P.; de Omena, P.M.; Goncalves-Souza, T.; Vieira, C.; Migliorini, G.H.; Kersch-Becker, M.N.F.; Bernabe, T.N.; Recalde, F.C.; Benavides-Gordillo, S.; Romero, G.Q. Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness. Oecologia 2020, 192, 745–753. [Google Scholar] [CrossRef]
- Kulkarni, S.S.; Dosdall, L.M.; Spence, J.R.; Willenborg, C.J. Seed Detection and Discrimination by Ground Beetles (Coleoptera: Carabidae) Are Associated with Olfactory Cues. PLoS ONE 2017, 12, 11. [Google Scholar] [CrossRef] [PubMed]
- Law, J.J.; Gallagher, R.S. The role of imbibition on seed selection by Harpalus pensylvanicus. Appl. Soil Ecol. 2015, 87, 118–124. [Google Scholar] [CrossRef]
- Niu, H.Y.; Chu, W.; Yi, X.F.; Zhang, H.M. Visual and auditory cues facilitate cache pilferage of Siberian chipmunks (Tamias sibiricus) under indoor conditions. Integr. Zool. 2019, 14, 354–365. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, J.F.; Vieira, E.M. Microhabitat selection for caching and use of potential landmarks for seed recovery by a neotropical rodent. J. Zool. 2016, 300, 274–280. [Google Scholar] [CrossRef]
- Griffin, C.A.M.; Thaler, J.S. Insect predators affect plant resistance via density- and trait-mediated indirect interactions. Ecol. Lett. 2006, 9, 335–343. [Google Scholar] [CrossRef]
- DeAngelis, K.M. Chemical communication connects soil food webs. Soil Biol. Biochem. 2016, 102, 48–51. [Google Scholar] [CrossRef]
- Paulsen, T.R.; Colville, L.; Kranner, I.; Daws, M.I.; Hogstedt, G.; Vandvik, V.; Thompson, K. Physical dormancy in seeds: A game of hide and seek? New Phytol. 2013, 198, 496–503. [Google Scholar] [CrossRef]
- Kielty, J.P.; AllenWilliams, L.J.; Underwood, N.; Eastwood, E.A. Behavioral responses of three species of ground beetle (Coleoptera: Carabidae) to olfactory cues associated with prey and habitat. J. Insect Behav. 1996, 9, 237–250. [Google Scholar] [CrossRef]
- Thomas, R.S.; Glen, D.M.; Symondson, W.O.C. Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus melanarius. Soil Biol. Biochem. 2008, 40, 207–216. [Google Scholar] [CrossRef]
- Thoming, G.; Solhaug, K.A.; Norli, H.R. Kairomone-assisted trap cropping for protecting spring oilseed rape (Brassica napus) from pollen beetles (Coleoptera: Nitidulidae). Pest Manag. Sci. 2020, 11. [Google Scholar] [CrossRef]
- Ma, C.; Cui, S.W.; Bai, Q.; Tian, Z.Y.; Zhang, Y.; Chen, G.M.; Gao, X.Y.; Tian, Z.Q.; Chen, H.S.; Guo, J.Y.; et al. Olfactory co-receptor is involved in host recognition and oviposition in Ophraella communa (Coleoptera: Chrysomelidae). Insect Mol. Biol. 2020, 10. [Google Scholar] [CrossRef]
- Baskin, C.C.; Baskin, J.M. Seeds, Ecology, Biogeography, and Evolution of Dormancy and Germination; Elsevier: San Diego, CA, USA, 1998. [Google Scholar]
- Linton, C.J.; Wright, S.J.L. Volatile organic-compounds—Mictrobiologicak aspects and some technological implications. J. Appl. Bacteriol. 1993, 75, 1–12. [Google Scholar] [CrossRef]
- Mattoo, A.K.; Suttle, J.C. Plant Hormone Ethylene; CRC Press: Boca Raton, FL, USA, 1991; p. 352. [Google Scholar]
- Honek, A.; Martinkova, Z.; Saska, P. Effect of size, taxonomic affiliation and geographic origin of dandelion (Taraxacum agg.) seeds on predation by ground beetles (Carabidae, Coleoptera). Basic Appl. Ecol. 2011, 12, 89–96. [Google Scholar] [CrossRef]
- Moles, A.T.; Warton, D.I.; Westoby, M. Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 2003, 84, 3148–3161. [Google Scholar] [CrossRef] [Green Version]
- Honek, A.; Martinkova, Z.; Jarosik, V. Ground beetles (Carabidae) as seed predators. Eur. J. Entomol. 2003, 100, 531–544. [Google Scholar] [CrossRef] [Green Version]
- Forsythe, T.G. Locomotion in ground beetles (Coleptera: Carabidae)—An interpretation of leg structure in functional terms. J. Zool. 1983, 200, 493–507. [Google Scholar]
- Acorn, J.H.; Ball, G.E. The mandibles of some adult ground beetles—Structure, function, and the evolution of herbivory (Coleptera: Carabidae). Can. J. Zool. Rev. Can. Zool. 1991, 69, 638–650. [Google Scholar] [CrossRef]
- Brown, J.S.; Venable, D.L. Evolutionary ecology of seed-bank annuals in temporally varying environments. Am. Nat. 1986, 127, 31–47. [Google Scholar] [CrossRef]
- Feeny, P.P. Plant apparency and chemical defense. Recent Adv. Phytochem. 1976, 10, 1–40. [Google Scholar]
- Thompson, K.; Band, S.R.; Hodgson, J.G. Seed size and shape predict persistence in soil. Funct. Ecol. 1993, 7, 236–241. [Google Scholar] [CrossRef] [Green Version]
- Bekker, R.M.; Bakker, J.P.; Grandin, U.; Kalamees, R.; Milberg, P.; Poschlod, P.; Thompson, K.; Willems, J.H. Seed size, shape and vertical distribution in the soil: Indicators of seed longevity. Funct. Ecol. 1998, 12, 834–842. [Google Scholar] [CrossRef]
- Thompson, K.; Bakker, J.; Bekker, R. The Soil Seed Banks of North West Europe: Methodology, Destiny and Longevity; Cambridge University Press: Cambridge, UK, 1997; p. 276. [Google Scholar]
- Azcarate, F.M.; Arqueros, L.; Sanchez, A.M.; Peco, B. Seed and fruit selection by harvester ants, Messor barbarus, in Mediterranean grassland and scrubland. Funct. Ecol. 2005, 19, 273–283. [Google Scholar] [CrossRef]
- Benvenuti, S. Natural weed seed burial: Effect of soil texture, rain and seed characteristics. Seed Sci. Res. 2007, 17, 211–219. [Google Scholar] [CrossRef]
- Bewley, J.D.; Black, M.J.B. Physiology and Biochemistry of Seeds in Relation to Germination; Springer: Berlin, Germany, 1982; p. 306. [Google Scholar]
- Lanza, J.; Schmitt, M.A.; Awad, A.B. Comparative chemistry of elaiosomes of 3 species of Trillium. J. Chem. Ecol. 1992, 18, 209–221. [Google Scholar] [CrossRef]
- Eigenbrode, S.D.; Jetter, R. Attachment to plant surface waxes by an insect predator. Integr. Comp. Biol. 2002, 42, 1091–1099. [Google Scholar] [CrossRef] [Green Version]
- Shao, S.Q.; Meyer, C.J.; Ma, F.S.; Peterson, C.A.; Bernards, M.A. The outermost cuticle of soybean seeds: Chemical composition and function during imbibition. J. Exp. Bot. 2007, 58, 1071–1082. [Google Scholar] [CrossRef] [Green Version]
- Mohamedyasseen, Y.; Barringer, S.A.; Splittstoesser, W.E.; Costanza, S. The role of seed coats in seed viability. Bot. Rev. 1994, 60, 426–439. [Google Scholar] [CrossRef]
- van der Meij, M.A.A.; Bout, R.G. Seed selection in the Java Sparrow (Padda oryzivora): Preference and mechanical constraint. Can. J. Zool. Rev. Can. Zool. 2000, 78, 1668–1673. [Google Scholar] [CrossRef]
- Rodgerson, L. Mechanical defense in seeds adapted for ant dispersal. Ecology 1998, 79, 1669–1677. [Google Scholar] [CrossRef]
- Benkman, C.W. The impact of tree squirrels (Tamiasciurus) on Limber pine seed dispersal adaptations. Evolution 1995, 49, 585–592. [Google Scholar] [CrossRef]
- Davis, A.S.; Schutte, B.J.; Iannuzzi, J.; Renner, K.A. Chemical and physical defense of weed seeds in relation to soil seedbank persistence. Weed Sci. 2008, 56, 676–684. [Google Scholar] [CrossRef]
- Janzen, D.H. Seed predation by animals. Curr. Contents/Agric. Biol. Environ. Sci. 1982, 465–492. [Google Scholar] [CrossRef]
- Hulme, P.E. Herbivory, plant regeneration, and species coexistence. J. Ecol. 1996, 84, 609–615. [Google Scholar] [CrossRef]
- Gaba, S.; Deroulers, P.; Bretagnolle, F.; Bretagnolle, V. Lipid content drives weed seed consumption by ground beetles (Coleopterea, Carabidae) within the smallest seeds. Weed Res. 2019, 59, 170–179. [Google Scholar] [CrossRef]
- Grubb, P.J.; Metcalfe, D.J.; Grubb, E.A.A.; Jones, G.D. Nitrogen-richness and protection of seeds in Australian tropical rainforest: A test of plant defence theory. Oikos 1998, 82, 467–482. [Google Scholar] [CrossRef]
- Bretagnolle, F.; Matejicek, A.; Gregoire, S.; Reboud, X.; Gaba, S. Determination of fatty acids content, global antioxidant activity and energy value of weed seeds from agricultural fields in France. Weed Res. 2016, 56, 78–95. [Google Scholar] [CrossRef]
- Pond, C.M. Ecology of Storage. In Encyclopedia of Biodiversity; Levin, S.M., Ed.; Academic Press: New York, NY, USA, 2013; p. 5504. [Google Scholar]
- Moles, A.T.; Westoby, M. Seed size and plant strategy across the whole life cycle. Oikos 2006, 113, 91–105. [Google Scholar] [CrossRef]
- Kubát, K.; Hrouda, L.; Chrtek, J.; Kaplan, Z.; Kirschner; Štěpánek, J. Klíč ke Květeně České Republiky; Academia: Praha, Czech Republic, 2002. [Google Scholar]
- Cerda, A.; Garcia-Fayos, P. The influence of seed size and shape on their removal by water erosion. Catena 2002, 48, 293–301. [Google Scholar] [CrossRef]
- Carvalho, A.P.; Malcata, F.X. Preparation of fatty acid methyl esters for gas-chromatographic analysis of marine lipids: Insight studies. J. Agric. Food Chem. 2005, 53, 5049–5059. [Google Scholar] [CrossRef]
- Stroescu, M.; Stoica-Guzun, A.; Ghergu, S.; Chira, N.; Jipa, I. Optimization of fatty acids extraction from Portulaca oleracea seed using response surface methodology. Ind. Crops Prod. 2013, 43, 405–411. [Google Scholar] [CrossRef]
- Mira, S.; Hill, L.M.; Gonzalez-Benito, M.E.; Ibanez, M.A.; Walters, C. Volatile emission in dry seeds as a way to probe chemical reactions during initial asymptomatic deterioration. J. Exp. Bot. 2016, 67, 1783–1793. [Google Scholar] [CrossRef]
- Bojnanský, V.; Fargašová, A. Atlas of Seeds and Fruits of Central and East-European Flora; Springer: Dordrecht, The Netherlands, 2007; p. 1046. [Google Scholar]
- Goslee, S.C.; Urban, D.L. The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 2007, 22, 1–19. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing. Available online: https://www.R-project.org/ (accessed on 3 November 2020).
- Lichstein, J.W. Multiple regression on distance matrices: A multivariate spatial analysis tool. Plant Ecol. 2007, 188, 117–131. [Google Scholar] [CrossRef]
- Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Szoecs, E.; Wagner, H. Vegan: Community Ecology Package. R Package Version 1.17–10. 2017. Available online: https://CRAN.R-project.org/package=vegan (accessed on 4 November 2020).
- Legendre, P.; Lapointe, F.J.; Casgrain, P. Modeling brain evolution from behavior—A permutational regretion approach. Evolution 1994, 48, 1487–1499. [Google Scholar] [CrossRef]
- Paarmann, W.; Faust, N.; Arndt, E.; Luchtrath, I.; Rohe, W. Constant seed size and mandible growth—A fundamental problem for granivorous ground beetle larvae (Coleoptera: Carabidae). Entomol. Fenn. 2006, 17, 334–339. [Google Scholar] [CrossRef]
- Larochelle, A. The Food of Carabid Beetles: (Coleoptera: Carabidae, Including Cicindelinae); Association des Entomologistes du Québec: Varennes, QC, Canada, 1990; p. 132. [Google Scholar]
- Zetto-Brandmayr, T. Spermophilus (Seed-Eating) Ground Beetles: First Comparison of the Diet and Ecology of the Harpaline General Harpalus and Ophonus (Col., Carabidae). In The Role of Ground Beetles in Ecological and Environmental Studies; Stork, N., Ed.; Intercept: Andover, UK, 1990; pp. 307–316. [Google Scholar]
- Jordan, L.S.; Jordan, J.L. Effects of prechilling on Convolvulus arvensis L. seed coat and germination. Ann. Bot. 1982, 49, 421–423. [Google Scholar] [CrossRef]
- Eynard, I. The Effect of Very Low Temperatures on Germination of Hard Seeds. In Herbage Abstracts; CAB International: Wallingford, UK, 1958; Volume 28, p. 1027. [Google Scholar]
- Raza, W.; Ling, N.; Liu, D.Y.; Wei, Z.; Huang, Q.W.; Shen, Q.R. Volatile Organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol. Res. 2016, 192, 103–113. [Google Scholar] [CrossRef]
- Rajagopal, B.S.; Daniels, L. Invertigation of Mercaptans, organic sulfides, and inorganic sulfur compounds as sulfur sources for the growth of methanogenic bacteria. Curr. Microbiol. 1986, 14, 137–144. [Google Scholar] [CrossRef]
- Schulz, S.; Dickschat, J.S. Bacterial volatiles: The smell of small organisms. Nat. Prod. Rep. 2007, 24, 814–842. [Google Scholar] [CrossRef]
- Nelson, E.B. The seed microbiome: Origins, interactions, and impacts. Plant Soil 2018, 422, 7–34. [Google Scholar] [CrossRef]
- Truyens, S.; Weyens, N.; Cuypers, A.; Vangronsveld, J. Bacterial seed endophytes: Genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 2015, 7, 40–50. [Google Scholar] [CrossRef]
Plants | Carabids | ||
---|---|---|---|
Species | Family | Species | Tribe |
Amaranthus retroflexus L. | Amaranthaceae | Acupalpus meridianus (Linnaeus) | Harpalini |
Arctium lappa L. | Asteraceae | Amara aenea (DeGeer) | Zabrini |
Arenaria serpyllifolia agg. | Caryophyllaceae | Amara anthobia (A. Villa et G.B. Villa) | Zabrini |
Bidens tripartita L. | Asteraceae | Amara apricaria (Paykull) | Zabrini |
Campanula trachelium L. | Campanulaceae | Amara aulica (Panzer) | Zabrini |
Capsella bursa-pastoris (L.) Med. | Brassicaceae | Amara bifrons (Gyllenhal) | Zabrini |
Chenopodium album L. | Amaranthaceae | Amara consularis (Duftschmid) | Zabrini |
Cichorium intybus L. | Asteraceae | Amara convexior (Stephens) | Zabrini |
Cirsium arvense (L.) Scop. | Asteraceae | Amara convexiuscula (Marsham) | Zabrini |
Consolida regalis S.F. Gray | Ranunculaceae | Amara eurynota (Panzer) | Zabrini |
Crepis biennis L. | Asteraceae | Amara familiaris (Duftschmid) | Zabrini |
Descurainia sophia (L.) Prantl | Brassicaceae | Amara ingenua (Duftschmid) | Zabrini |
Fumaria officinalis L. | Papaveraceae | Amara litorea (C.G.Thomson) | Zabrini |
Galinsoga parviflora Cav. | Asteraceae | Amara montivaga (Sturm) | Zabrini |
Galium aparine L. | Rubiaceae | Amara ovata (Fabricius) | Zabrini |
Lapsana communis L. | Asteraceae | Amara sabulosa (Audient-Serville) | Zabrini |
Leonurus cardiaca L. | Lamiaceae | Amara similata (Gyllenhal) | Zabrini |
Lepidium ruderale L. | Brassicaceae | Amara spreta (Dejean) | Zabrini |
Melilotus albus Med. | Fabaceae | Anisodactylus signatus (Panzer) | Harpalini |
Potentilla argentea L. | Rosaceae | Calathus ambiguus (Paykull) | Sphodrini |
Silene latifolia alba (Mill.) Greut. et Burdet | Caryophyllaceae | Calathus fuscipes (Goeze) | Sphodrini |
Sisymbrium loeselii L. | Brassicaceae | Harpalus affinis (Schrank) | Harpalini |
Stellaria media (L.) Vill. | Caryophyllaceae | Harpalus atratus (Latreille) | Harpalini |
Taraxacum officinale agg. | Asteraceae | Harpalus distinguendus (Duftschmid) | Harpalini |
Thlaspi arvense L. | Brassicaceae | Harpalus honestus (Duftschmid) | Harpalini |
Tripleurospermum inodorum (L.) Schultz-Bip. | Asteraceae | Harpalus luteicornis (Duftschmid) | Harpalini |
Urtica dioica L. | Urticaceae | Harpalus rubripes (Duftschmid) | Harpalini |
Viola arvensis Murray | Violaceae | Harpalus signaticornis (Duftschmid) | Harpalini |
Harpalus subcylindricus (Dejean) | Harpalini | ||
Ophonus azureus (Fabricius) | Harpalini | ||
Parophonus maculicornis (Duftschmid) | Harpalini | ||
Pseudoophonus griseus (Panzer) | Harpalini | ||
Pseudoophonus rufipes (DeGeer) | Harpalini | ||
Pterostichus melanarius (Illiger) | Pterostichini | ||
Stenolophus teutonus (Schrank) | Harpalini | ||
Trechus quadristriatus (Schrank) | Trechini | ||
Zabrus tenebrioides (Goeze) | Zabrini |
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Foffová, H.; Ćavar Zeljković, S.; Honěk, A.; Martinková, Z.; Tarkowski, P.; Saska, P. Which Seed Properties Determine the Preferences of Carabid Beetle Seed Predators? Insects 2020, 11, 757. https://doi.org/10.3390/insects11110757
Foffová H, Ćavar Zeljković S, Honěk A, Martinková Z, Tarkowski P, Saska P. Which Seed Properties Determine the Preferences of Carabid Beetle Seed Predators? Insects. 2020; 11(11):757. https://doi.org/10.3390/insects11110757
Chicago/Turabian StyleFoffová, Hana, Sanja Ćavar Zeljković, Alois Honěk, Zdenka Martinková, Petr Tarkowski, and Pavel Saska. 2020. "Which Seed Properties Determine the Preferences of Carabid Beetle Seed Predators?" Insects 11, no. 11: 757. https://doi.org/10.3390/insects11110757
APA StyleFoffová, H., Ćavar Zeljković, S., Honěk, A., Martinková, Z., Tarkowski, P., & Saska, P. (2020). Which Seed Properties Determine the Preferences of Carabid Beetle Seed Predators? Insects, 11(11), 757. https://doi.org/10.3390/insects11110757