Selective top-down control of epiphytic biomass by amphipods from Posidonia oceanica meadows: implications for ecosystem functioning
DOI:
https://doi.org/10.26496/bjz.2015.49Keywords:
epiphyte grazing, mesograzers, Amphipoda, nutrient cycling, Posidonia oceanicaAbstract
Mediterranean Posidonia oceanica meadows shelter an important biomass and biodiversity of amphipod crustaceans that graze on epiphytes. However, their actual significance for ecosystem functional processes is hard to estimate, due to the lack of adequate data. Here, a field microcosm-based inclusion experiment was used to test if three of the dominant taxa of the amphipod community (Apherusa chiereghinii, Dexamine spiniventris and Gammarus spp.) could exert top-down control on seagrass leaf epiphytes. Influence of amphipod activity on nutrient availability for the host species was also investigated. All grazer taxa significantly reduced biomasses of erect macroalgae and erect sessile animals present on leaves. None of them consumed encrusting epiflora or epifauna. This selective top-down control could have important implications for the structure of the epiphytic community on leaves of P. oceanica, which is one of the most diverse and abundant of all seagrass species. Grazing activity of all taxa caused higher N content of seagrass leaves, likely through amphipod excretion and/or sloppy feeding. Since P. oceanica meadows often grow in oligotrophic zones where plant growth can be nutrient-limited, this N enrichment could enhance seagrass production. Overall, the ecological interaction between P. oceanica and amphipods could be seen as a facultative mutualistic relationship. Our results suggest that amphipod mesograzers are key-elements in some of the functional processes regulating these complex and yet endangered ecosystems, which are essential components of Mediterranean coastal zones.References
Alcoverro T, Romero J, Duarte CM & Lopez NI (1997). Spatial and temporal variations in nutrient limitation of seagrass Posidonia oceanica growth in the NW Mediterranean. Marine Ecology Progress Series, 146: 155-161.
Alsterberg C, Eklof JS, Gamfeldt L, Havenhand JN & Sundback K (2013). Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proceedings of the National Academy of Sciences of the United States of America, 110(21): 8603-8608.
Bay D (1984). A field study of the growth dynamics and productivity of Posidonia oceanica (L.) Delile in Calvi Bay, Corsica. Aquatic Botany, 20(1-2): 43-64.
Bell JD & Harmelin-Vivien ML (1983). Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. 2. Feeding habits. Tethys, 11: 1-14.
Bellan-Santini D (1999) Ordre des Amphipodes (Amphipoda Latreille, 1816). In: Forest J (ed), Traité de Zoologie - Anatomie, Systématique, Biologie (Pierre-P. Grassé). Tome VII, Fascicule III A : Crustacés Péracarides. Institut Océanographique de Monaco, Monaco: 93-176.
Bethoux J & Copin-Montégut G (1986). Biological fixation of atmospheric nitrogen in the Mediterranean Sea. Limnology and Oceanography, 31(6): 1353-1358.
Borowitzka MA, Lavery P & van Keulen M (2006) Epiphytes of seagrasses. In: Larkum AWD, Orth RJ & Duarte CM (eds), Seagrasses: Biology, Ecology and Conservation. Springer: 441-461.
Bracken MES, Gonzalez-Dorantes CA & Stachowicz JJ (2007). Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology, 88(9): 2211-2219.
Brawley HS (1992) Mesoherbivores. In: John DM, Hawkins SJ & Price JH (eds), Plant-Animal Interactions in the Marine Benthos. Clarendon Press, Oxford: 235-263.
Buia MC, Gambi MC & Zupo V (2000). Structure and functioning of Mediterranean seagrass ecosystems: an overview. Biologia Marina Mediterranea, 7: 167-190.
Caine EA (1980). Ecology of two littoral species of caprellid amphipods (Crustacea) from Washington, USA. Marine Biology, 56(4): 327-335.
Cebrian J, Enriquez S, Fortes M, Agawin N, Vermaat JE & Duarte CM (1999). Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Botanica Marina, 42: 123-128.
Cook K, Vanderklift MA & Poore AGB (2011). Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Marine Ecology Progress Series, 442: 263-269.
Douglass JG, Duffy JE, Spivak C & Richardson JP (2007). Nutrient versus consumer control of community structure in a Chesapeake Bay eelgrass habitat. Marine Ecology Progress Series, 348: 71-83.
Duarte CM (2002). The future of seagrass meadows. Environmental Conservation, 29(2): 192-206.
Duffy JE & Harvilicz AM (2001). Species-specific impacts of grazing amphipods in an eelgrass-bed community. Marine Ecology Progress Series, 223: 201-211.
Duffy JE, Richardson JP & Canuel EA (2003). Grazer diversity effects on ecosystem functioning in seagrass beds. Ecology Letters, 6: 637-645.
Duffy JE, MacDonald KS, Rhode JM & Parker JD (2001). Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology, 82(9): 2417-2434.
Gacia E, Costalago D, Prado P, Piorno D & Tomas F (2009). Mesograzers in Posidonia ocea-nica meadows: an update of data on gastropod-epiphyte-seagrass interactions. Botanica Marina, 52(5).
Gambi MC, Lorenti M, Russo GF, Scipione MB & Zupo V (1992). Depth and seasonal distribution of some groups of the vagile fauna of the Posidonia oceanica leaf stratum: Structural and trophic analyses. Marine Ecology, 13(1): 17-39.
Gobert S, Kyramarios M, Lepoint G, Pergent-Martini C & Bouquegneau JM (2003). Variations at different spatial scales of Posidonia oceanica (L.) Delile beds; effects on the physico-chemical parameters of the sediment. Oceanologica Acta, 26(2): 199-207.
Gobert S, Cambridge ML, Velimirov B, Pergent G, Lepoint G, Bouquegneau JM, Dauby P, Pergent-Martini C & Walker DI (2006) Biology of Posidonia. In: Larkum AWD, Orth RJ & Duarte CM (eds), Seagrasses : Biology, Ecology and Conservation: 387-408.
Hays CG (2005). Effect of nutrient availability, grazer assemblage and seagrass source population on the interaction between Thalassia testudinum (turtle grass) and its algal epiphytes. Journal of Experimental Marine Biology and Ecology, 314(1): 53-68.
Howard RK (1982). Impact of feeding activities of epibenthic amphipods on surface-fouling of eelgrass blades. Aquatic Botany, 14: 91-97.
Hughes AR, Bando KJ, Rodriguez LF & Williams SL (2004). Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Marine Ecology Progress Series, 282: 87-99.
Hurd CL, Durante KM, Chia FS & Harrison PJ (1994). Effect of bryozoan colonization on inorganic nitrogen acquisition by the kelps Agarum fimbriatum and Macrocystis integrifolia. Marine Biology, 121(1): 167-173.
Jaschinski S & Sommer U (2008). Functional diversity of mesograzers in an eelgrass–epiphyte system. Marine Biology, 154(3): 475-482.
Jaschinski S & Sommer U (2010). Positive effects of mesograzers on epiphytes in an eelgrass system. Marine Ecology Progress Series, 401: 77-85.
Jaschinski S, Flöder S & Sommer U (2010). Consumer identity, abundance and nutrient concentration affect epiphyte diversity in an experimental eelgrass system. Oikos, 119(11): 1745-1754.
Jernakoff P & Nielsen J (1997). The relative importance of amphipod and gastropod grazers in Posidonia sinuosa meadows. Aquatic Botany, 56(3-4): 183-202.
Jernakoff P, Brearley A & Nielsen J (1996). Factors affecting grazer-epiphytes interactions in temperate seagrass meadows. Oceanography and Marine Biology: an Annual Review, 34: 109-162.
Lefcheck JS, van Montfrans J, Orth RJ, Schmitt EL, Duffy JE & Luckenbach MW (2014). Epifaunal invertebrates as predators of juvenile bay scallops (Argopecten irradians). Journal of Experimental Marine Biology and Ecology, 454: 18-25.
Lepoint G, Gobert S, Dauby P & Bouquegneau JM (2004). Contributions of benthic and plankto-nic primary producers to nitrate and ammonium uptake fluxes in an nutrient-poor shallow coastal area (Corsica, NW Mediterranean). Journal of Experimental Marine Biology and Ecology, 302: 107-122.
Lepoint G, Nyssen F, Gobert S, Dauby P & Bouquegneau J-M (2000). Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Marine Biology, 136: 513-518.
Lepoint G, Jacquemart J, Bouquegneau JM, Demoulin V & Gobert S (2007). Field measure-ments of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). Journal of Phycology, 4(2): 208-218.
Mazzella L & Russo GF (1989). Grazing effect of two Gibbula species (Mollusca, Archaeogastropoda) on the epiphytic community of Posidonia oceanica leaves. Aquatic Botany, 35: 353-373.
Mazzella L, Scipione MB & Buia MC (1989). Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica meadow. Marine Ecology, 10(2): 107-129.
Michel L (2011). Multidisciplinary study of trophic diversity and functional role of amphipod crustaceans associated to Posidonia oceanica meadows. PhD in Sciences thesis, University of Liège, Belgium.
Michel L, Lepoint G, Dauby P & Sturaro N (2010). Sampling methods for amphipods of Posidonia oceanica meadows: a comparative study. Crustaceana, 83(1): 39-47.
Michel LN, Dauby P, Gobert S, Graeve M, Nyssen F, Thelen N & Lepoint G (in press). Dominant amphipods of Posidonia oceanica seagrass meadows display considerable trophic diversity. Marine Ecology.
Myers JA & Heck KLJ (2013). Amphipod control of epiphyte load and the concomitant effects on shoalgrass Halodule wrightii biomass. Marine Ecology Progress Series, 483: 133-142.
Neckles HA, Wetzel RL & Orth RJ (1993). Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia, 93: 285-295.
Peduzzi P (1987). Dietary preferences and carbon absorption by two marine gastropods, Gibbula umbilicaris (Linné) and Jujubinus striatus (Linné). Marine Ecology, 8(4): 359-370.
Pinnegar JK & Polunin NVC (2000). Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia, 122(3): 399-409.
Poore AG, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA & Duffy JE (2012). Global patterns in the impact of marine herbivores on benthic primary producers. Ecological Letters, 15(8): 912-922.
Sturaro N, Lepoint G, Vermeulen S & Gobert S (2015). Multiscale variability of amphipod assemblages in Posidonia oceanica meadows. Journal of Sea Research, 95: 258-271.
Valentine JF & Duffy JE (2006) The central role of grazing in seagrass ecology. In: Larkum AWD, Orth RJ & Duarte CM (eds), Seagrasses: Biology, Ecology and Conservation. Springer: 463-501.
Vizzini S (2009). Analysis of the trophic role of Mediterranean seagrasses in marine coastal ecosystems: a review. Botanica Marina, 52(5): 383-393.
Vizzini S, Sarà G, Michener RH & Mazzola A (2002). The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecologica, 23: 277-285.
Whalen MA, Duffy JE & Grace JB (2013). Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology, 94(2): 510-520.
Downloads
Published
How to Cite
Issue
Section
License
All published papers will be put on-line as high resolution PDF’s. Copyright thus remains with the authors. All manuscripts will be licensed under a Creative Commons Attribution 3.0 License https://creativecommons.org/licenses/by/4.0/.