Feeding preferences of amphipod crustaceans Ampithoe ramondi and Gammarella fucicola for Posidonia oceanica seeds and leaves
DOI:
https://doi.org/10.3989/scimar.04892.06BKeywords:
herbivory, mechanical traits, nutritional quality, invertebrate food choice, crustacean, gammaridAbstract
The functional importance of herbivory in seagrass beds is highly variable among systems. In Mediterranean seagrass meadows, macroherbivores, such as the fish Sarpa salpa and the sea urchin Paracentrotus lividus, have received most research attention, so published evidence highlights their importance in seagrass consumption. The role of small crustaceans in seagrass consumption remains less studied in the region. Herbivory on Posidonia oceanica seeds has not previously been reported. In turn, crustacean herbivory on P. oceanica leaves is broadly recognized, although the species feeding on the seagrass are mostly unknown (except for Idotea baltica). This work evaluates P. oceanica consumption by two species of amphipod crustaceans commonly found in seagrass meadows. Ampithoe ramondi and Gammarella fucicola actively feed on P. oceanica leaves and seeds. Both species preferred seeds to leaves only when the seed coat was damaged. This study provides the first direct evidence of consumption of P. oceanica seeds by the two named amphipod crustaceans, and confirms that they also consume leaves of this seagrass species.
Downloads
References
Andersson S., Persson M., Moksnes P.-O., et al. 2009. The role of the amphipod Gammarus locusta as a grazer on macroalgae in Swedish seagrass meadows. Mar. Biol. 156: 969-981. https://doi.org/10.1007/s00227-009-1141-1
Aranwela N., Sanson G., Read J. 1999. Methods of assessing leaf-fracture properties. New Phytol. 144: 369-393. https://doi.org/10.1046/j.1469-8137.1999.00506.x
Balestri E., Gobert S., Lepoint G., et al. 2009. Seed nutrient content and nutritional status of Posidonia oceanica seedlings in the northwestern Mediterranean Sea. Mar. Ecol. Prog. Ser. 388: 99-109. https://doi.org/10.3354/meps08104
Barnes R.S.K. 2017. Patterns of benthic invertebrate biodiversity in intertidal seagrass in Moreton Bay, Queensland. Reg. Stud. Mar. Sci. 15: 17-25. https://doi.org/10.1016/j.rsma.2017.07.003
Bellan-Santini D., Karaman G., Krapp-Schickel G., et al. 1982. The Amphipoda of the Mediterranean. Mem. Inst. Oceanogr. (Monaco) 13: 1-364.
Cabaço S., Santos R. 2012. Seagrass reproductive effort as an ecological indicator of disturbance. Ecol. Indic. 23: 116-122. https://doi.org/10.1016/j.ecolind.2012.03.022
Caldwell E., Read J., Sanson G.D. 2016. Which leaf mechanical traits correlate with insect herbivory among feeding guilds? Ann. Bot. 117: 349-361. https://doi.org/10.1093/aob/mcv178 PMid:26715468 PMCid:PMC4724051
Celdrán D., Marín A. 2013. Seed photosynthesis enhances Posidonia oceanica seedling growth. Ecosphere 4: 1-11. https://doi.org/10.1890/ES13-00104.1
Conacher C.A., Poiner I.R., Butler J., et al. 1994a. Germination, storage and viability testing of seeds of Zostera capricorni Aschers. from a tropical bay in Australia. Aquat. Bot. 49: 47-58. https://doi.org/10.1016/0304-3770(94)90005-1
Conacher C.A., Poiner I.R., O'Donohue M. 1994b. Morphology, flowering and seed production of Zostera capricorni Aschers. in subtropical Australia. Aquat. Bot. 49: 33-46. https://doi.org/10.1016/0304-3770(94)90004-3
Cruz-Rivera E., Friedlander M. 2011. Feeding preferences of mesograzers on aquacultured Gracilaria and sympatric algae. Aquaculture 322-323: 218-222. https://doi.org/10.1016/j.aquaculture.2011.09.035 PMid:22711945 PMCid:PMC3375704
Cruz-Rivera E., Hay M.E. 2000. Can quantity replace quality ? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81: 201-219. https://doi.org/10.1890/0012-9658(2000)081[0201:CQRQFC]2.0.CO;2
Cruz-Rivera E., Hay M.E. 2003. Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol. Monogr. 73: 483-506. https://doi.org/10.1890/0012-9615(2003)073[0483:PNQIWC]2.0.CO;2
Dall W., Smith D.M., Moore L.E. 1992. The composition of Zostera capricorni seeds: a seasonal natural food of juvenile Penaeus esculentus Haswell (Penaeidae: Decapoda). Aquaculture 101: 75-83. https://doi.org/10.1016/0044-8486(92)90233-B
Davis A.S., Schutte B.J., Iannuzzi J., et al. 2008. Chemical and physical defense of weed seeds in relation to soil seedbank persistence. Weed Sci. 56: 676-684. https://doi.org/10.1614/WS-07-196.1
De los Santos C.B., Onoda Y., Vergara J.J., et al. 2016. A comprehensive analysis of mechanical and morphological traits in temperate and tropical seagrass species. Mar. Ecol. Prog. Ser. 551: 81-94. https://doi.org/10.3354/meps11717
Delefosse M., Povidisa K., Poncet D., et al. 2016. Variation in size and chemical composition of seeds from the seagrass Zostera marina-Ecological implications. Aquat. Bot. 131: 7-14. https://doi.org/10.1016/j.aquabot.2016.02.003
Díaz-Almela E., Marbà N., Alvarez E., et al. 2006. Patterns of seagrass (Posidonia oceanica) flowering in the Western Mediterranean. Mar. Biol. 148: 723-742. https://doi.org/10.1007/s00227-005-0127-x
Duffy J.E., Hay M.E. 1994. Herbivore resistance to seaweed chemical defense: the roles of mobility and predation risk. Ecology 75: 1304-1319. https://doi.org/10.2307/1937456
Edgar G.J., Shaw C. 1995a. The production and trophic ecology of shallow-water fish assemblages in southern Australia II. Diets of fishes and trophic relationships between fishes and benthos at Western Port, Victoria. J. Exp. Mar. Bio. Ecol. 194: 83-106. https://doi.org/10.1016/0022-0981(95)00084-4
Edgar G.J., Shaw C. 1995b. The production and trophic ecology of shallow-water fish assemblages in southern Australia 3. General relationships between sediments, seagrasses, invertebrates and fishes. J. Exp. Mar. Bio. Ecol. 194: 107-131. https://doi.org/10.1016/0022-0981(95)00085-2
Fishman J.R., Orth R.J. 1996. Effects of predation on Zostera marina L. seed abundance. J. Exp. Mar. Bio. Ecol. 198: 11-26. https://doi.org/10.1016/0022-0981(95)00176-X
Fourqurean J.W., Zieman J.C., Powell G.V.N. 1992. Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Mar. Biol. 114: 57-65.
Freeman B.C., Beattie G.A. 2008. An overview of plant defenses against pathogens and herbivores. Plant Path. Microbiol. Publ. 94 https://doi.org/10.1094/PHI-I-2008-0226-01
Gruner D.S., Smith J.E., Seabloom E.W., et al. 2008. A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol. Lett. 11: 740-755. https://doi.org/10.1111/j.1461-0248.2008.01192.x PMid:18445030
Guidetti P. 2000. Invertebrate borers in the Mediterranean sea grass Posidonia oceanica: Biological impact and ecological implications. J. Mar. Biol. Assoc. UK 80: 725-730. https://doi.org/10.1017/S0025315400002551
Heck K.L., Valentine J.F. 2006. Plant-herbivore interactions in seagrass meadows. J. Exp. Mar. Bio. Ecol. 330: 420-436. https://doi.org/10.1016/j.jembe.2005.12.044
Hernán G., Ramajo L., Basso L., et al. 2016. Seagrass (Posidonia oceanica) seedlings in a high-CO2 world: from physiology to herbivory. Sci. Rep. 6: 38017. https://doi.org/10.1038/srep38017 PMid:27905514 PMCid:PMC5131316
Hernán G., Ortega M.J., Gándara A.M., et al. 2017. Future warmer seas: Increased stress and susceptibility to grazing in seedlings of a marine habitat-forming species. Glob. Chang. Biol. 23: 4530-4543. https://doi.org/10.1111/gcb.13768 PMid:28544549
Hillebrand H. 2009. Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J. Phycol. 45: 798-806. https://doi.org/10.1111/j.1529-8817.2009.00702.x PMid:27034208
Ibanez S., Lavorel S., Puijalon S., et al. 2013. Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers. Funct. Ecol. 27: 479-489. https://doi.org/10.1111/1365-2435.12058
Jaschinski S., Aberle N., Gohse-Reimann S., et al. 2009. Grazer diversity effects in an eelgrass-epiphyte-microphytobenthos system. Oecologia 159: 607-615. https://doi.org/10.1007/s00442-008-1236-2 PMid:19082631 PMCid:PMC2757588
Jernakoff P., Nielsen J. 1997. The relative importance of amphipod and gastropod grazers in Posidonia sinuosa meadows. Aquat. Bot. 56: 183-202. https://doi.org/10.1016/S0304-3770(96)01112-6
Jiménez-Ramos R., Egea L.G., Ortega M.J., et al. 2017. Global and local disturbances interact to modify seagrass palatability. PLoS ONE 12: e0183256. https://doi.org/10.1371/journal.pone.0183256 PMid:28813506 PMCid:PMC5558941
Kendrick G.A., Waycott M., Carruthers T.J.B., et al. 2012. The central role of dispersal in the maintenance and persistence of seagrass populations. Bioscience 62: 56-65. https://doi.org/10.1525/bio.2012.62.1.10
Lepoint G., Cox A.-S.S., Dauby P., et al. 2006. Food sources of two detritivore amphipods associated with the seagrass Posidonia oceanica leaf litter. Mar. Biol. Res. 2: 355-365. https://doi.org/10.1080/17451000600962797
Lepoint G., Jacquemart J., Bouquegneau J.M., et al. 2007. Field measurements of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). J. Phycol. 43: 208-218. https://doi.org/10.1111/j.1529-8817.2007.00322.x
Loques F., Caye G., Meinesz A. 1990. Germination in the marine phanerogam Zostera noltii Hornemann at Golfe Juan, French Mediterranean. Aquat. Bot. 38: 249-260. https://doi.org/10.1016/0304-3770(90)90009-A
Michel L., Dauby P., Gobert S., et al. 2014. Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity. Mar. Ecol. 36: 969-981. https://doi.org/10.1111/maec.12194
Michel L.N., Dauby P., Dupont A., et al. 2015. Selective top-down control of epiphytic biomass by amphipods from Posidonia oceanica meadows: implications for ecosystem functioning. Belg. J. Zool. 145: 83-93. https://doi.org/10.26496/bjz.2015.49
Moore E.., Hovel K. 2010. Relative influence of habitat complexity and proximity to patch edges on seagrass epifaunal communities. Oikos 119: 1299-1311. https://doi.org/10.1111/j.1600-0706.2009.17909.x
Nakamura Y., Sano M. 2005. Comparison of invertebrate abundance in a seagrass bed and adjacent coral and sand areas at Amitori Bay, Iriomote Island, Japan. Fish. Sci. 71: 543-550. https://doi.org/10.1111/j.1444-2906.2005.00998.x
Nakaoka M. 2002. Predation on seeds of seagrasses Zostera marina and Zostera caulescens by a tanaid crustacean Zeuxo sp. Aquat. Bot. 72: 99-106. https://doi.org/10.1016/S0304-3770(01)00213-3
Navarro-Barranco C., Tierno-de-Figueroa J.M., Guerra-García J.M., et al. 2013. Feeding habits of amphipods (Crustacea: Malacostraca) from shallow soft bottom communities: Comparison between marine caves and open habitats. J. Sea Res. 78: 1-7. https://doi.org/10.1016/j.seares.2012.12.011
Onoda Y., Schieving F., Anten N.P.R. 2008. Effects of light and nutrient availability on leaf mechanical properties of Plantago major: A conceptual approach. Ann. Bot. 101: 727-736. https://doi.org/10.1093/aob/mcn013 PMid:18272529 PMCid:PMC2710173
Onoda Y., Westoby M., Adler P.B., et al. 2011. Global patterns of leaf mechanical properties. Ecol. Lett. 14: 301-312. https://doi.org/10.1111/j.1461-0248.2010.01582.x PMid:21265976
Orth R.J., Heck K.L., Tunbridge D.J. 2002. Predation on seeds of the seagrass Posidonia australis in Western Australia. Mar. Ecol. Prog. Ser. 244: 81-88. https://doi.org/10.3354/meps244081
Orth R.J., Kendrick G.A., Marion S.R. 2006. Predation on Posidonia australis seeds in seagrass habitats of Rottnest Island, Western Australia: Patterns and predators. Mar. Ecol. Prog. Ser. 313: 105-114. https://doi.org/10.3354/meps313105
Orth R.J., Kendrick G.A., Marion S.R. 2007. Posidonia australis seed predation in seagrass habitats of Two Peoples Bay, Western Australia. Aquat. Bot. 86: 83-85. https://doi.org/10.1016/j.aquabot.2006.09.012
Peirano A, Niccolai I., Mauro R., et al. 2001. Seasonal grazing and food preference of herbivores in a Posidonia oceanica meadow. Sci. Mar. 65: 367-374. https://doi.org/10.3989/scimar.2001.65n4367
Poore A.G.B., Campbell A.H., Coleman R.A., et al. 2012. Global patterns in the impact of marine herbivores on benthic primary producers. Ecol. Lett. 15: 912-922. https://doi.org/10.1111/j.1461-0248.2012.01804.x PMid:22639820
Prado P., Alcoverro T., Romero J. 2010. Influence of nutrients in the feeding ecology of seagrass (Posidonia oceanica L.) consumers: A stable isotopes approach. Mar. Biol. 157: 715-724. https://doi.org/10.1007/s00227-009-1355-2
Reynolds L.K., Carr L.A., Boyer K.E. 2012. A non-native amphipod consumes eelgrass inflorescences in San Francisco Bay. Mar. Ecol. Prog. Ser. 451: 107-118. https://doi.org/10.3354/meps09569
Rhoades D.F., Cates R.G. 1976. Toward a general theory of plant antiherbivore chemistry. In: Wallace J.W., Mansell R.L. (eds) Biochemical Interaction Between Plants and Insects. Recent Advances in Phytochemistry book series vol. 10. Springer, Boston, pp. 168-213. https://doi.org/10.1007/978-1-4684-2646-5_4
Rodgerson L. 1998. Mechanical defense in seeds adapted for ant dispersal. Ecology 79: 1669-1677. https://doi.org/10.1890/0012-9658(1998)079[1669:MDISAF]2.0.CO;2
Rueda J.L., Salas C., Urra J., et al. 2009. Herbivory on Zostera marina by the gastropod Smaragdia viridis. Aquat. Bot. 90: 253-260. https://doi.org/10.1016/j.aquabot.2008.10.003
Sanchez-Jerez P., Barberá-Cebrián C., Ramos Esplá A. 1999. Comparison of the epifauna spatial distribution in Posidonia oceanica, Cymodocea nodosa and unvegetated bottoms: Importance of meadow edges. Acta Oecologica 20: 391-405. https://doi.org/10.1016/S1146-609X(99)00128-9
Silberhorn G.M., Orth R.J., Moore K.A. 1983. Anthesis and seed production in Zostera marina L. (eelgrass) from the Chesepeak Bay. Aquat. Bot. 15: 133-144. https://doi.org/10.1016/0304-3770(83)90024-4
Sokal R.R., Rohlf F.J. 1981. Biometry, W.H. Freeman and Company, New York, 859 pp.
Sturaro N., Lepoint G., Vermeulen S., et al. 2015. Multiscale variability of amphipod assemblages in Posidonia oceanica meadows. J. Sea Res. 95: 258-271. https://doi.org/10.1016/j.seares.2014.04.011
Thayer G.W., Bjorndal K.A., Ogden J.C., et al. 1984. Role of larger herbivores in seagrass community. Estuaries 7: 351-376. https://doi.org/10.2307/1351619
Uchida M., Miyoshi T., Kaneniwa M., et al. 2014. Production of 16.5% v/v ethanol from seagrass seeds. J. Biosci. Bioeng. 118: 646-650. https://doi.org/10.1016/j.jbiosc.2014.05.017 PMid:24969514
Valentine J.F., Duffy J.E. 2006. The central role of grazing in seagrass ecology. In: Larkum A.W.D. et al. (eds) Seagrasses: Biology, Ecology and Conservation. Springer, Dordrecht, pp. 463-501. https://doi.org/10.1007/1-4020-2983-7_20
Veldman J.W., Greg Murray K., Hull A.L., et al. 2007. Chemical defense and the persistence of pioneer plant seeds in the soil of a tropical cloud forest. Biotropica 39: 87-93. https://doi.org/10.1111/j.1744-7429.2006.00232.x
Vergés A., Becerro M.A., Alcoverro T., et al. 2007. Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions. Oecologia 151: 675-686. https://doi.org/10.1007/s00442-006-0606-x PMid:17120055
Vergés A., Alcoverro T., Romero J. 2011. Plant defences and the role of epibiosis in mediating within-plant feeding choices of seagrass consumers. Oecologia 166: 381-390. https://doi.org/10.1007/s00442-010-1830-y PMid:21053016
Wassenberg T.J. 1990. Seasonal feeding on Zostera capricorni seeds by juvenile Penaeus esculentus (Crustacea: Decapoda) in Moreton Bay, Queensland. Mar. Freshw. Res. 41: 301-310. https://doi.org/10.1071/MF9900301
Wigand C., Coolidge Churchill A. 1988. Laboratory studies on eelgrass seed and seedling predation. Estuaries 11: 180-183. https://doi.org/10.2307/1351970
Zakhama-Sraieb R., Sghaier Y.-R., Charfi-Cheikhrouha F. 2006. Is amphipod diversity related to the quality of Posidonia oceanica beds? Biol. Mar. Mediterr. 13: 174-180.
Zakhama-Sraieb R., Sghaier Y.R., Charfi-Cheikhrouha F. 2011. Community structure of amphipods on shallow Posidonia oceanica meadows off Tunisian coasts. Helgol. Mar. Res. 65: 203-209. https://doi.org/10.1007/s10152-010-0216-1
Published
How to Cite
Issue
Section
License
Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read here the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
