Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non-consumptive effects of predators
2010; Wiley; Volume: 56; Issue: 2 Linguagem: Inglês
10.1111/j.1365-2427.2010.02497.x
ISSN1365-2427
Autores Tópico(s)Isotope Analysis in Ecology
ResumoFreshwater BiologyVolume 56, Issue 2 p. 302-310 Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non-consumptive effects of predators HARUKO YOSHIE, HARUKO YOSHIE Faculty of Science, Nara Women’s University, Nara, JapanSearch for more papers by this authorYOICHI YUSA, YOICHI YUSA Faculty of Science, Nara Women’s University, Nara, JapanSearch for more papers by this author HARUKO YOSHIE, HARUKO YOSHIE Faculty of Science, Nara Women’s University, Nara, JapanSearch for more papers by this authorYOICHI YUSA, YOICHI YUSA Faculty of Science, Nara Women’s University, Nara, JapanSearch for more papers by this author First published: 15 September 2010 https://doi.org/10.1111/j.1365-2427.2010.02497.xCitations: 11 Yoichi Yusa, Faculty of Science, Nara Women’s University, Kitauoya-nishi, Nara 630-8506, Japan. E-mail: [email protected] Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Summary 1. Density- and trait-mediated indirect interactions (DMIIs and TMIIs, respectively) in food chains play crucial roles in community structure and processes. However, factors affecting the relative strength of these interactions are poorly understood, including in widespread and important freshwater rice ecosystems. 2. We studied the strength of DMIIs and TMIIs in a food chain involving a predator (the Reeve’s turtle Chinemys reevesii), its herbivorous prey (the apple snail Pomacea canaliculata) and a plant (rice Oryza sativa) in outdoor containers simulating rice fields. We also evaluated consumptive and non-consumptive effects of the predator on the snail. We removed a fixed proportion of snails every 2 days to simulate prey consumption and introduced a caged turtle that was fed daily with snails to simulate non-consumptive effects. 3. Direct consumptive effects increased growth of the remaining snails and their per capita feeding rate. Moreover, consumptive and non-consumptive effects, and their interaction, affected the proportion of snails buried in the soil. This interaction was presumably because increasing food availability per snail induced their self-burying behaviour. 4. Both DMIIs and TMIIs affected the number of rice plants remaining, whereas their interaction term was not significant. 5. In summary, density dependence and interactions between consumptive and non-consumptive effects influenced snail growth and behaviour, respectively. However, no cascading effects of these complicated interactions on rice plants were detected. References Aizaki K. & Yusa Y. (2009) Field observations of the alarm response to crushed conspecifics in the freshwater snail Pomacea canaliculata: effects of habitat, vegetation, and body size. Journal of Ethology, 27, 175–180. 10.1007/s10164-008-0103-2 Web of Science®Google Scholar Aizaki K. & Yusa Y. (2010) Learned predator recognition in a freshwater snail, Pomacea canaliculata. Malacologia, 52, 21–29. 10.4002/040.052.0102 Web of Science®Google Scholar Bourne G.R. & Berlin J.A. (1982) Predicting Pomacea dolioides (Reeve) (Prosobranchia: Ampullariidae) weights from linear measurements of their shells. Veliger, 24, 367–370. Web of Science®Google Scholar Carlsson N.O.L., Brönmark C. & Hansson L.A. (2004a) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology, 85, 1575–1580. 10.1890/03-3146 Web of Science®Google Scholar Carlsson N.O.L., Kestrup Å., Mårtensson M. & Nyström P. (2004b) Lethal and non-lethal effects of multiple indigenous predators on the invasive golden apple snail (Pomacea canaliculata). Freshwater Biology, 49, 1269–1279. 10.1111/j.1365-2427.2004.01269.x Web of Science®Google Scholar Ecological Society of Japan (2002) Handbook of Alien Species in Japan. Chijin-shokan, Tokyo (in Japanese). Google Scholar Estoy G.F., Yusa Y., Wada T., Sakurai H. & Tsuchida K. (2002) Size and age at first copulation and spawning of the apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae). Applied Entomology and Zoology, 37, 199–205. 10.1303/aez.2002.199 Web of Science®Google Scholar Fang L., Wong P.K., Lin L., Lan C. & Qiu J.-W. (2010) Impact of invasive apple snails in Hong Kong on wetland macrophytes, nutrients, phytoplankton and filamentous algae. Freshwater Biology, 55, 1191–1204. 10.1111/j.1365-2427.2009.02343.x CASWeb of Science®Google Scholar Grafen A. & Hails R. (2002) Modern Statistics for the Life Sciences. Oxford University Press, Oxford. Google Scholar Griffin C.A.M. & Thaler J.S. (2006) Insect predators affect plant resistance via density- and trait-mediated interactions. Ecology Letters, 9, 338–346. 10.1111/j.1461-0248.2005.00880.x PubMedWeb of Science®Google Scholar Halwart M. (1994) The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat. International Journal of Pest Management, 40, 199–206. 10.1080/09670879409371882 Web of Science®Google Scholar Ichinose K. (2002) Influence of age and body size on alarm responses in a freshwater snail Pomacea canaliculata. Journal of Chemical Ecology, 28, 2017–2027. 10.1023/A:1020749911877 CASPubMedWeb of Science®Google Scholar Ichinose K., Yusa Y. & Yoshida K. (2003) Alarm response of hatchlings of the apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae), to aqueous extracts of other individuals. Ecological Research, 18, 213–219. 10.1046/j.1440-1703.2003.00548.x Web of Science®Google Scholar Japan Meteorological Agency (2009) Website of Japan Meteorological Agency. Available at: http://www.jma.go.jp/jma/indexe.html. Google Scholar Joshi R.C. & Sebastian L.S. (2006) Global Advances in Ecology and Management of Golden Apple Snails. Philippine Rice Research Institute, Nueva Ecija, Philippines. Google Scholar Kanno H. & Fujita Y. (2003) Induced systemic resistance to rice blast fungus in rice plants infested by white-backed planthopper. Entomologia Experimentalis et Applicata, 107, 155–158. 10.1046/j.1570-7458.2003.00045.x Web of Science®Google Scholar Kanno H., Satoh M., Kimura T. & Fujita Y. (2005) Some aspects of induced resistance to rice blast fungus, Magnaporthe grisea, in rice plant infested by white-backed planthopper, Sogatella furcifera. Applied Entomology and Zoology, 40, 91–97. 10.1303/aez.2005.91 Web of Science®Google Scholar Kunert G. & Weisser W.W. (2003) The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism. Oecologia, 135, 304–312. 10.1007/s00442-003-1185-8 PubMedWeb of Science®Google Scholar Lonsdale W.M. (1999) Global patterns of plant invasions and the concept of invasibility. Ecology, 80, 1522–1536. 10.1890/0012-9658(1999)080[1522:GPOPIA]2.0.CO;2 Web of Science®Google Scholar Lowe S., Browne M., Bouduelas S. & De Pooter M. (2000) 100 of the World’s Worst Invasive Alien Species. The Invasive Species Specialist Group, IUCN (Available at: http://www.issg.org/). Google Scholar Luttbeg B., Rowe L. & Mangel M. (2003) Prey state and experimental design affect relative size of trait- and density-mediated indirect effects. Ecology, 84, 1140–1150. 10.1890/0012-9658(2003)084[1140:PSAEDA]2.0.CO;2 Web of Science®Google Scholar Morton B., Chan K. & Britton J.C. (1995) Hunger overcomes fear in Nassarius festivus, a scavenging gastropod on Hong Kong shores. Journal of Molluscan Studies, 61, 55–63. 10.1093/mollus/61.1.55 Web of Science®Google Scholar Naylor R. (1996) Invasions in agriculture: assessing the cost of the golden apple snail in Asia. Ambio, 25, 443–448. Web of Science®Google Scholar Okada K., Uchida T. & Uchida S. (1965) New Illustrated Encyclopedia of the Fauna of Japan, Vol 3. Hokuryu-kan, Tokyo (in Japanese). Google Scholar Okuyama T. & Bolker B.M. (2007) On quantitative measures of indirect interactions. Ecology Letters, 10, 264–271. 10.1111/j.1461-0248.2007.01019.x CASPubMedWeb of Science®Google Scholar Ozawa A. & Makino T. (1997) The influence of shell size, snail density and water depth in paddy fields on injury of young rice seedling by the apple snails, Pomacea canaliculata (Lamarck). Bulletin of Shizuoka Agricultural Experimental Station, 42, 23–29 (in Japanese with English summary). Google Scholar Peacor S.D. & Werner E.E. (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proceedings of the National Academy of Sciences of the United States of America, 98, 3904–3908. 10.1073/pnas.071061998 CASPubMedWeb of Science®Google Scholar Preisser E.L., Bolnick D.I. & Benard M.F. (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions Ecology, 86, 501–509. 10.1890/04-0719 Web of Science®Google Scholar Rosenberg M.S., Adams D.C. & Gurevitch J. (2000) MetaWin: Statistical Software for Meta-analysis, Version 2. Sinauer, Massachusetts. Google Scholar Schmitz O.J., Beckerman A.P. & O’Brien K.M. (1997) Behaviorally-mediated trophic cascades: effects of predation risk on food web interactions. Ecology, 78, 1388–1399. 10.1890/0012-9658(1997)078[1388:BMTCEO]2.0.CO;2 Web of Science®Google Scholar Schmitz O.J., Krivan V. & Ovadia O. (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters, 7, 153–163. 10.1111/j.1461-0248.2003.00560.x Web of Science®Google Scholar Settle W.H., Ariawan H., Astuti E.T., Cahyana W., Hakim A.L., Hindayana D., Lestari A.S., Pajarningsih & Sartanto (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology, 77, 1975–1988. 10.2307/2265694 Web of Science®Google Scholar Soto R.E., Castilla J.C. & Bozinovic F. (2005) The impact of physiological demands on foraging decision under predation risk: a test with the whelk Acanthina monodon. Ethology, 111, 1044–1049. 10.1111/j.1439-0310.2005.01107.x Web of Science®Google Scholar Takashima T. (1988) A Handbook of Rice Culture Practice. Nobunkyo, Tokyo (in Japanese). Google Scholar Tamburi N.E. & Martín P.R. (2009) Reaction norms of size and age at maturity of Pomacea canaliculata (Gastropoda: Ampullariidae) under a gradient of food deprivation. Journal of Molluscan Studies, 75, 19–26. 10.1093/mollus/eyn031 Web of Science®Google Scholar Tanaka K., Watanabe T., Higuchi H., Miyamoto K., Yusa Y., Kiyonaga T., Kiyota H., Suzuki Y. & Wada T. (1999) Density-dependent growth and reproduction of the apple snail, Pomacea canaliculata: a density manipulation experiment in a paddy field. Researches on Population Ecology, 41, 253–262. 10.1007/s101440050029 Web of Science®Google Scholar Trussell G.C., Ewanchuk P.J. & Bertness M.D. (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecology Letters, 5, 241–245. 10.1046/j.1461-0248.2002.00304.x Web of Science®Google Scholar Trussell G.C., Ewanchuk P.J., Bertness M.D. & Silliman B.R. (2004) Trophic cascade in rocky shore tide pool: distinguishing lethal and nonlethal effects. Oecologia, 139, 427–432. 10.1007/s00442-004-1512-8 PubMedWeb of Science®Google Scholar Trussell G.C., Ewanchuk P.J. & Matassa C.M. (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecology Letters, 9, 1245–1252. 10.1111/j.1461-0248.2006.00981.x PubMedWeb of Science®Google Scholar Turner A.M. (2004) Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions. Oikos, 104, 561–569. 10.1111/j.0030-1299.2004.12615.x Web of Science®Google Scholar Turner A.M., Bernot R.J. & Boes C.M. (2000) Chemical cues modify species interactions: the ecological consequences of predator avoidance by freshwater snails. Oikos, 88, 148–158. 10.1034/j.1600-0706.2000.880117.x CASWeb of Science®Google Scholar Une Y. (1999) The apple snail. In: Growing Rice without Herbicides (Ed. M. Inaba), pp. 163–171. Nobunkyo, Tokyo (in Japanese). Google Scholar Wada T. (2002) Influences of changing from transplanting to direct seeding on the status of some pest species. In: Direct Seedling: Research Strategies and Opportunities (Eds S. Pandey, M. Mortimer, L. Wade, T.P. Tuong, K. Lopez & B. Hardy), pp. 341–348. IRRI, Los Banõs, Philippines. Google Scholar Wada T., Ichinose K., Yusa Y. & Sugiura N. (2004) Decrease in density of the apple snail Pomacea canaliculata (Lamarck) (Gastropoda: Ampullariidae) in paddy fields after crop rotation with soybean, and its population growth during the crop season. Applied Entomology and Zoology, 39, 367–372. 10.1303/aez.2004.367 Web of Science®Google Scholar Walzer A. & Schausberger P. (2009) Non-consumptive effects of predatory mites on thrips and its host plant. Oikos, 118, 934–940. 10.1111/j.1600-0706.2008.17299.x Web of Science®Google Scholar Werner E.E. & Peacor S.D. (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology, 84, 1083–1100. 10.1890/0012-9658(2003)084[1083:AROTII]2.0.CO;2 Web of Science®Google Scholar Wojdak J.M. & Luttbeg B. (2005) Relative strengths of trait-mediated and density-mediated indirect effects of a predator vary with resource levels in a freshwater food chain. Oikos, 111, 592–598. 10.1111/j.0030-1299.2005.13869.x Web of Science®Google Scholar Yoshida K., Hoshikawa K., Wada T. & Yusa Y. (2009) Life cycle of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) inhabiting Japanese paddy fields. Applied Entomology and Zoology, 44, 465–474. 10.1303/aez.2009.465 Web of Science®Google Scholar Yoshie H. & Yusa Y. (2008) Effects of predation on the exotic freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) by the indigenous turtle Chinemys reevesii (Testudines: Geoemydidae). Applied Entomology and Zoology, 43, 475–482. 10.1303/aez.2008.475 Web of Science®Google Scholar Yusa Y. (2006) Predators of the introduced apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae): their effectiveness and utilization in biological control. In: Global Advances in Ecology and Management of Golden Apple Snails (Eds R.C. Joshi & L.S. Sebastian), pp. 345–361. Philippine Rice Research Institute, Nueva Ecija, Philippines. Google Scholar Yusa Y., Sugiura N. & Wada T. (2006) Predatory potential of freshwater animals on an invasive agricultural pest, the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae), in southern Japan. Biological Invasions, 8, 137–147. 10.1007/s10530-004-1790-4 Web of Science®Google Scholar Citing Literature Volume56, Issue2February 2011Pages 302-310 ReferencesRelatedInformation
Referência(s)