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Seasonal fluctuation in food sources of herbivorous gastropods in a subtropical seagrass bed estimated by stable isotope analysis

Published online by Cambridge University Press:  19 December 2018

Kenta Nakamoto Open the ORCID record for Kenta Nakamoto [Opens in a new window] ,
Jun Hayakawa ,
Tomohiko Kawamura ,
Naoya Ohtsuchi ,
Hideaki Yamada ,
Takashi Kitagawa  and
Yoshiro Watanabe
Kenta Nakamoto*
Affiliation:
International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
Jun Hayakawa
Affiliation:
International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
Tomohiko Kawamura
Affiliation:
International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
Naoya Ohtsuchi
Affiliation:
International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
Hideaki Yamada
Affiliation:
Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, 1551-8, Taira-machi, Nagasaki, Nagasaki 851-2213, Japan
Takashi Kitagawa
Affiliation:
International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo, 2-106-1, Akahama, Otsuchi, Iwate 028-1102, Japan
Yoshiro Watanabe
Affiliation:
Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5, Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
*
Author for correspondence: Kenta Nakamoto, [email protected]
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Abstract

Various herbivorous invertebrates in seagrass beds are considered to be generalists in food use and their diets may temporally fluctuate according to the availability of food sources. We assessed whether food sources of herbivorous gastropods vary in a subtropical seagrass bed in Nagura Bay, Ishigaki Island, where coexisting seaweeds grow densely in spring but minimally in summer. Abundant gastropods and their possible food sources were collected in spring and summer of 2013 and 2015, and their stable carbon and nitrogen isotope ratios were measured. Between the two seasons, each possible food source had similar isotopic values, but all the herbivorous gastropod species in summer were more enriched in 13C than the gastropod samples in spring. The mixing models in SIAR (Stable Isotope Analysis in R) showed that the total contribution rates of seaweeds, i.e. rhodophytes, phaeophytes and chlorophytes, for all herbivorous gastropod species decreased from spring to summer; in contrast, the contribution rate of seagrasses increased. Linear Mixed Models showed that the seasonal variation in δ13C of the herbivorous gastropods was larger than that of the possible food sources, adding further evidence to the seasonal change in food sources of the herbivorous gastropods. This seasonal change in food use appears to correspond to the change in seaweed biomass, suggesting that herbivorous gastropods flexibly change their diets depending on food availability.

Keywords

Herbivorous invertebratesseagrass bedsubtropical areaδ13Cδ15N
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 5 , August 2019 , pp. 1119 - 1125
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Agawin, N, Duarte, CM, Fortes, MD, Uri, JS and Vermaat, JE (2001) Temporal changes in the abundance, leaf growth and photosynthesis of three co-occurring Philippine seagrasses. Journal of Experimental Marine Biology and Ecology 260, 217–239.Google Scholar
Bates, D, Maechler, M, Bolker, BM and Walker, SC (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Brearley, A and Walker, DI (1995) Isopod miners in the leaves of two Western Australian Posidonia species. Aquatic Botany 52, 163–181.Google Scholar
Davis, BC and Fourqurean, JW (2001) Competition between the tropical alga, Halimeda incrassata, and the seagrass, Thalassia testudinum. Aquatic Botany 71, 217–232.Google Scholar
Doropoulos, C, Hyndes, GA, Lavery, PS and Tuya, F (2009) Dietary preferences of two seagrass inhabiting gastropods: allochthonous vs autochthonous resources. Estuarine, Coastal and Shelf Science 83, 13–18.Google Scholar
Douglass, JG, Duffy, JE and Bruno, JF (2008) Herbivore and predator diversity interactively affect ecosystem properties in an experimental marine community. Ecology Letters 11, 598–608.Google Scholar
Douglass, JG, Duffy, JE and Canuel, EA (2011) Food web structure in a Chesapeake Bay eelgrass bed as determined through gut contents and 13C and 15N isotope analysis. Estuaries and Coasts 34, 701–711.Google Scholar
Duarte, CM and Chiscano, CL (1999) Seagrass biomass and production: a reassessment. Aquatic Botany 65, 159–174.Google Scholar
Duffy, JE (2006) Biodiversity and the functioning of seagrass ecosystems. Marine Ecology Progress Series 311, 233–250.Google Scholar
Folch, J, Lees, M and Sloane Stanley, GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497–509.Google Scholar
Fukuoka, K and Yamada, H (2015) Food habits of juvenile tuskfishes (Choerodon schoenleinii and C. anchorago) in relation to food availability in the shallow waters of Ishigaki Island, Southwestern Japan. Fisheries Science 81, 331–344.Google Scholar
Heijs, FM (1985) The seasonal distribution and community structure of the epiphytic algae on Thalassia hemprichii (Ehrenb.) Aschers. from Papua New Guinea. Aquatic Botany 21, 295–324.Google Scholar
Horinouchi, M and Sano, M (2000) Food habits of fishes in a Zostera marina bed at Aburatsubo, Central Japan. Ichthyological Research 47, 163–173.Google Scholar
Jaschinski, S, Brepohl, DC and Sommer, U (2008) Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Marine Ecology Progress Series 358, 103–114.Google Scholar
Jernakoff, P, Brearley, A and Nielsen, J (1996) Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceanography and Marine Biology: An Annual Review 34, 109–162.Google Scholar
Jeong, SJ, Suh, H and Kang, C (2012) Trophic diversity in amphipods within a temperate eelgrass ecosystem as determined by gut contents and C and N isotope analysis. Marine Biology 159, 1943–1954.Google Scholar
Kharlamenko, VI, Kiyashko, SI, Imbs, AB and Vyshkvartzev, DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Marine Ecology Progress Series 220, 103–117.Google Scholar
Lebreton, B, Richard, P, Galois, R, Radenac, G, Brahmia, A, Colli, G, Grouazel, M, André, C, Guillou, G and Blanchard, GF (2012) Food sources used by sediment meiofauna in an intertidal Zostera noltii seagrass bed: a seasonal stable isotope study. Marine Biology 159, 1537–1550.Google Scholar
Lewis, FG (1987) Crustacean epifauna of seagrass and macroalgae in Apalachee Bay, Florida, USA. Marine Biology 94, 219–229.Google Scholar
Mateo, MA, Serrano, O, Serrano, L and Michener, RH (2008) Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157, 105–115.Google Scholar
McIntyre, PB and Flecker, AS (2006) Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148, 12–21.Google Scholar
Michel, LN, Dauby, P, Gobert, S, Graeve, M, Nyssen, F, Thelen, N and Lepoint, G (2015) Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity. Marine Ecology 36, 969–981.Google Scholar
Minagawa, M and Wada, E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.Google Scholar
Mittermayr, A, Fox, SE and Sommer, U (2014) Temporal variation in stable isotope composition (δ13C, δ15N and δ34S) of a temperate Zostera marina food web. Marine Ecology Progress Series 505, 95–105.Google Scholar
Nakamura, Y, Horinouchi, M, Nakai, T and Sano, M (2003) Food habits of fishes in a seagrass bed on a fringing coral reef at Iriomote Island, southern Japan. Ichthyological Research 50, 15–22.Google Scholar
Nakaoka, M (2005) Plant–animal interactions in seagrass beds: ongoing and future challenges for understanding population and community dynamics. Population Ecology 47, 167–177.Google Scholar
Nienhuis, PH and Van Ierland, ET (1978) Consumption of eelgrass, Zostera marina, by birds and invertebrates during the growing season in Lake Grevelingen (SW Netherlands). Netherlands Journal of Sea Research 12, 180–194.Google Scholar
Parnell, AC, Inger, R, Bearhop, S and Jackson, AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5, e9672.Google Scholar
Paula, J, Ecosta, PF, Martins, A and Gove, D (2001) Patterns of abundance of seagrasses and associated infaunal communities at Inhaca Island, Mozambique. Estuarine, Coastal and Shelf Science 53, 307–318.Google Scholar
Pillans, RD, Franklin, CE and Tibbetts, IR (2004) Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. Journal of Fish Biology 64, 297–309.Google Scholar
Post, DM, Layman, CA, Arrington, DA, Takimoto, G, Quattrochi, J and Montana, CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.Google Scholar
R Development Core Team (2017) https://www.r-project.org/.Google Scholar
Short, F, Carruthers, T, Dennison, W and Waycott, M (2007) Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology 350, 3–20.Google Scholar
Thomas, SM and Crowther, TW (2015) Predicting rates of isotopic turnover across the animal kingdom: a synthesis of existing data. Journal of Animal Ecology 84, 861–870.Google Scholar
Titlyanov, EA, Titlyanova, TV, Li, X, Hansen, GI and Huang, H (2014) Seasonal changes in the intertidal algal communities of Sanya Bay (Hainan Island, China). Journal of the Marine Biological Association of the United Kingdom 94, 879–893.Google Scholar
Tsai, C, Wong, S, Chang, J, Hwang, R, Dai, C, Yu, Y, Shyu, Y, Sheu, F and Lee, T (2004) Macroalgal assemblage structure on a coral reef in Nanwan Bay in southern Taiwan. Botanica Marina 47, 439–453.Google Scholar
Tytlyanov, EA, Titlyanova, TV, Huang, H and Li, X (2014) Seasonal changes in benthic algal communities of the upper subtidal zone in Sanya Bay (Hainan Island, China). Journal of the Marine Biological Association of the United Kingdom 94, 51–64.Google Scholar
Unabia, CR (2011) The snail Smaragdia bryanae (Neritopsina, Neritidae) is a specialist herbivore of the seagrass Halophila hawaiiana (Alismatidae, Hydrocharitaceae). Invertebrate Biology 130, 100–114.Google Scholar
Valentine, JF and Heck, KL Jr (1999) Seagrass herbivory: evidence for the continued grazing of marine grasses. Marine Ecology Progress Series 176, 291–302.Google Scholar
Van Montfrans, J, Orth, RJ and Vay, SA (1982) Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquatic Botany 14, 75–89.Google Scholar
Vander Zanden, MJ, Clayton, MK, Moody, EK, Solomon, CT and Weidel, BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS ONE 10, e0116182.Google Scholar
Vonk, JA, Christianen, MJ and Stapel, J (2008) Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows. Estuarine, Coastal and Shelf Science 79, 653–660.Google Scholar
Won, N, Kawamura, T, Onitsuka, T, Hayakawa, J, Watanabe, S, Horii, T, Takami, H and Watanabe, Y (2007) Community and trophic structures of abalone Haliotis diversicolor habitat in Sagami Bay, Japan. Fisheries Science 73, 1123–1136.Google Scholar
Yamada, H, Hayakawa, J, Nakamoto, K, Kawamura, T and Kon, K (2016 a) Effects of artificial seaweed on vulnerability of two gastropod species (Cerithium zonatum and Clypeomorus bifasciata) to carnivorous crab Calappa hepatica. Nippon Suisan Gakkaishi 82, 33–35.Google Scholar
Yamada, H, Shimabukuro, H, Hayakawa, J, Nakamoto, K, Kawamura, T and Kon, K (2016 b) Assessment of feeding preference for subtropical macrophytes in young Siganus fuscescens. Nippon Suisan Gakkaishi 82, 631–633.Google Scholar
Zapata, O and McMillan, C (1979) Phenolic acids in seagrasses. Aquatic Botany 7, 307–317.Google Scholar