Abstract
The loss of biodiversity by the replacement of invasive species could lead to the loss of functional traits that maintain certain ecosystem services (ES). The ES method provides a conceptual framework to value changes of functional traits related to this loss of biodiversity. The Caribbean Sea offers a multifaceted seascape to evaluate this approach as native seagrass species (Thalassia testudinum, Syringodium filiforme or Halodule wrightii) cohabit this region together with the invasive seagrass Halophila stipulacea, native to the Indian Ocean. The functional traits of native seagrass species in the Caribbean are compared to different traits of H. stipulacea observed worldwide with the aim of evaluating the dimensions of this change in terms of the ES that seagrass meadows provide in the Caribbean. Under a changing seascape due to climate change and anthropogenic pressures that have driven the disappearance of most seagrass meadows in the Caribbean, we explore how this invasive seagrass could play a role in restoration attempts as a pioneer species where native species have been lost. The potential unintended consequences of the presence of H. stipulacea to replace services of native species are also noted.
Similar content being viewed by others
References
Abed-Navandi D, Dworschak PC (2005) Food sources of tropical thalassinidean shrimps: a stable-isotope study. Mar Ecol Prog Ser 291:159–168
Alexandre A, Georgiou D, Santos R (2014) Inorganic nitrogen acquisition by the tropical seagrass Halophila stipulacea. Mar Ecol 35:387–394
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193
Becking LE, van Bussel TCJM, Debrot AO, Christianen MJA (2014) First record of a Caribbean green turtle (Chelonia mydas) grazing on invasive seagrass (Halophila stipulacea). Caribb J Sci 48:162–163
Biermann C, Anderson RM (2017) Conservation, biopolitics, and the governance of life and death. Geogr Compass 11:e12329
Bremner J (2008) Species’ traits and ecological functioning in marine conservation and management. J Exp Mar Biol Ecol 366:37–47
Carruthers TJB, van Tussenbroek BI, Dennison WC (2005) Influence of submarine springs and wastewater on nutrient dynamics of Caribbean seagrass meadows. Estuar Coast Shelf Sci 64:191–199
Charles H, Dukes KS (2008) Impacts of invasive species on ecosystem services. In: Nentwig W (ed) Biological invasions. Ecological studies (analysis and synthesis), vol 193. Springer, Berlin, pp 217–237
Chiquillo KL, Barber PH, Willette DA (2018) Fruits and flowers of the invasive seagrass Halophila stipulacea in the Caribbean Sea. Bot Mar. https://doi.org/10.1515/bot-2018-0052
Christianen MJA, Smulders FOH, Engel MS, Nava MI, Willis S, Debrot AO, Palsbøll PJ, Vonk JA, Becking LE (2019) Megaherbivores may impact expansion of invasive seagrass in the Caribbean. J Ecol 107:45–57
Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260
Costanza R, de Groot R, Braat L, Kubiszewski I, Fioramonti L, Sutton P, Farber S, Grasso M (2017) Twenty years of ecosystem services: how far have we come and how far do we still need to go? Ecosyst Serv 28:1–16
Cullen-Unsworth LC, Nordlund L, Paddock J, Baker S, McKenzie LJ, Unsworth RKF (2014) Seagrass meadows globally as a coupled social–ecological system: implications for human wellbeing. Mar Pollut Bull 83:387–397
de Groot RS, Wilson MA, Boumans RM (2002) A typology for the classification, description and valuation of ecosystems functions, goods and services. Ecol Econ 41:393–408
de la Torre-Castro M, Rönnbäck P (2004) Links between humans and seagrasses-an example from tropical East Africa. Ocean Coast Manage 47:361–387
Debrot AO, Hylkema A, Vogelaar W, Meesters HWG, Engel MS, de Leon R, Prud’homme van Reine WF, Nagelkerken I (2012) Baseline surveys of Lac Bay benthic and fish communities, Bonaire. Institute for Marine Resources and Ecosystems Studies Report C129/12
Diaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–665
Didham RK, Tylianakis JM, Hutchison MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends Ecol Evol 20:470–474
Dorenbosch M, Verberk W, Nagelkerken I, van der Velde G (2007) Influence of habitat configuration on connectivity between fish assemblages of Caribbean seagrass beds, mangroves and coral reefs. Mar Ecol Prog Ser 334:103–116
Dromard CR, Vaslet A, Gautier F, Bouchon-Navaro Y, Harmelin-Vivien M, Bouchon C (2017) Resource use by three juvenile scarids (Cryptotomus roseus, Scarus iseri, Sparisoma radians) in Caribbean seagrass beds. Aquat Bot 136:1–8
Duarte CM (2000) Marine biodiversity and ecosystem services: an elusive link. J Exp Mar Biol Ecol 250:117–131
Ellis S (2016) Potentially invasive sea grass found in Christiansted Harbor. St. Thomas Source, Sep 22
Enríquez S, Marbà N, Duarte CM, van Tussenbroek BI, Reyes-Zavala G (2001) Effects of seagrass Thalassia testudinum on sediment redox. Mar Ecol Prog Ser 219:149–158
Fonseca MS, Cahalan JA (1992) A preliminary evaluation of wave attenuation by 4 species of seagrass. Estuar Coast Shelf Sci 35:565–576
Fourqurean JW, Manuel S, Coates KA, Kenworthy WJ, Smith SR (2010) Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda. Mar Ecol Prog Ser 419:223–232
Gambi MC, Barbieri F, Bianchi CN (2009) New record of the alien seagrass Halophila stipulacea (Hydrocharitaceae) in the western Mediterranean: a further clue to changing Mediterranean Sea biogeography. Mar Biodivers Rec 2:e84
Georgiou D, Alexandre A, Luis J, Santos R (2016) Temperature is not a limiting factor for the expansion of Halophila stipulacea throughout the Mediterranean Sea. Mar Ecol Prog Ser 544:159–167
Gillis LG, Bouma TJ, Jones CG, van Katwijk MM, Nagelkerken I, Jeuken CJL, Herman PMJ, Ziegler D (2014) Potential for landscape-scale positive interactions among tropical marine ecosystems. Mar Ecol Prog Ser 503:289–303
Glenn E, Comarazamy D, González JE, Smith T (2015) Detection of recent regional sea surface temperature warming in the Caribbean and surrounding region. Geophys Res Lett 42:6785–6792
Herrera-Silveira JA, Cebrian J, Hauxwell J, Ramirez-Ramirez J, Ralph P (2010) Evidence of negative impacts of ecological tourism on turtlegrass (Thalassia testudinum) beds in a marine protected area of the Mexican Caribbean. Aquat Ecol 44:23–31
Hershner C, Havens KJ (2008) Managing invasive aquatic plants in a changing system: strategic consideration of ecosystem services. Conserv Biol 22:544–550
Holzer KK, Rueda JL, McGlathery KJ (2011) Caribbean seagrasses as a food source for the emerald neritid Smaragdia viridis. Am Malacol Bull 29:63–67
Hylkema A, Vogelaar W, Meesters HWG, Nagelkerken I, Debrot AO (2015) Fish species utilization of contrasting sub-habitats distributed along an ocean-to-land environmental gradient in a tropical mangrove and seagrass lagoon. Estuar Coasts 38:1448–1465
Jackson EL, Rowden AA, Attrill MJ, Bossey SJ, Jones MB (2001) The importance of seagrass beds as a habitat for fishery species. Oceanogr Mar Biol Annu Rev 39:269–303
Jax K (2005) Function and “functioning” in ecology: what does it mean? Oikos 111:641–648
Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190
Kairo M, Ali B (2003) Invasive species threats in the Caribbean region. Report to the Nature Conservancy. CAB International
Kannan RRR, Arumugam R, Anantharaman P (2010) Antibacterial potential of three seagrasses against human pathogens. Asian Pac J Trop Med 3:890–893
Kerninon F (2012) Première actions de mis en place d’un réseau d’observation desherbiers de l’Outre-mer (First actions in setting up an overseas seagrass moni-toring network). Dissertation, Universite de Bretagne Occidentale (in French)
Kilminster K, McMahon K, Waycott M, Kendrick GA, Scanes P, McKenzie L, O’Brien KR, Lyons M, Ferguson A, Maxwell P et al (2015) Unravelling complexity in seagrass systems for management: Australia as a microcosm. Sci Total Environ 534:97–109
Koltes KH, Opishinski TB (2009) Patterns of water quality and movement in the vicinity of Carrie Bow Cay, Belize. Smithson Contrib Mar Sci 38:379–390
Lee KS, Park JI (2008) An effective transplanting technique using shells for restoration of Zostera marina habitats. Mar Pollut Bull 56:1015–1021
Lefcheck JS, Orth RJ, Dennison WC, Wilcox DJ, Murphy RR, Keisman J, Gurbisz C, Hannam M, Landry JB, Moore KA et al (2018) Long-term nutrient reductions lead to the unprecedented recovery of a temperate coastal region. PNAS 115:3658–3662
Linton D, Fisher T (2004) CARICOMP-Caribbean coastal marine productivity program: 1993–2003. Caribbean Coastal Marine Productivity (CARICOMP) Program. CARICOMP
Lipkin Y (1975) Halophila stipulacea in Cyprus and Rhodes, 1967–1970. Aquat Bot 1:309–320
Lipkin Y (1979) Quantitative aspects of seagrass communities, particularly of those dominate by Halophila stipulacea, in Sinai (Northern Red Sea). Aquat Bot 7:119–128
MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55
Maréchal J-P, Meesters EH, Vedie F, Hellio C (2013) Occurrence of the alien seagrass Halophila stipulacea in Martinique (French West Indies). Mar Biodivers Rec 6:e127
Maxwell PS, Eklöf JS, van Katwijk MM, O’Brien KR, de la Torre-Castro M, Boström C, Bouma TJ, Krause-Jensen D, Unsworth RKF, van Tussenbroek BI et al (2017) The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems—a review. Biol Rev 92:1521–1538
Moberg F, Rönnbäck P (2003) Ecosystem services of the tropical seascape: interactions, substitutions and restoration. Ocean Coast Manag 46:27–46
Moran KL, Bjorndal KA (2005) Simulated green turtle grazing affects structure and productivity of seagrass pastures. Mar Ecol Prog Ser 305:235–247
Murdoch TJT, Glasspool AF, Outerbridge M, Ward J, Manuel S, Gray J, Nash A, Coates KA, Pitt J, Fourqurean JW et al (2007) Large-scale decline in offshore seagrass meadows in Bermuda. Mar Ecol Prog Ser 339:123–130
Nagelkerken I, van der Velde G, Gorissen MW, Meijer GJ, Van’t Hof T, den Hartog C (2000) Importance of mangroves, seagrass beds and the shallow coral reef as a nursery for important coral reef fishes, using a visual census technique. Estuar Coast Shelf Sci 51:31–44
Nagelkerken I, Roberts CM, van der Velde G, Dorenbosch M, van Riel MC, de la Morinière EC, Nienhuis PH (2002) How important are mangroves and seagrass beds for coral-reef fish? The nursery hypothesis tested on an island scale. Mar Ecol Prog Ser 244:299–305
Nordlund LM, Koch EW, Barbier EB, Creed JC (2016) Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 11(10):e0163091
Ogden JC, Gladfelter EH (1983) Coral reefs, seagrass beds and mangroves: their interactions in the coastal zones of the Caribbean. UNESCO Report Marine Science 23. UNESCO, Paris
Olinger LK, Heidmann SL, Durdall AN, Howe C, Ramseyer T, Thomas SG, Lasseigne DN, Brown EJ, Cassell JS, Donihe MM et al (2017) Altered juvenile fish communities associated with invasive Halophila stipulacea seagrass habitats in the U.S. Virgin Islands. PLoS ONE 12:e0188386
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996
Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504
Peterson BJ, Heck KL (2001) Positive interactions between suspension-feeding bivalves and seagrass—a facultative mutualism. Mar Ecol Prog Ser 213:143–155
Potouroglou M, Bull JC, Krauss KW, Kennedy HA, Fusi M, Daffonchio D, Mangora MM, Githaiga MN, Diele K, Huxham M (2017) Measuring the role of seagrasses in regulating sediment surface elevation. Sci Rep 7:11917
Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939
Rogers CS, Beets J (2001) Degradation of marine ecosystems and decline of fishery resources in marine protected areas in the US Virgin Islands. Environ Conserv 28:312–322
Rogers CS, Willette DA, Miller J (2014) Rapidly spreading seagrass invades the Caribbean with unknown ecological consequences. Front Ecol Environ 12:546–547
Ruiz H, Ballantine DL (2004) Occurrence of the seagrass Halophila stipulacea in the tropical west Atlantic. Bull Mar Sci 75:131–135
Ruiz H, Ballantine DL, Sabater J (2017) Continued spread of the seagrass Halophila stipulacea in the Caribbean: Documentation in Puerto Rico and the British Virgin Islands. Gulf Caribb Res 28:SC5–SC7
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Scheibling RE, Patriquin DG, Filbee-Dexter K (2018) Distribution and abundance of the invasive seagrass Halophila stipulacea and associated benthic macrofauna in Carriacou, Grenadines, Eastern Caribbean. Aquat Bot 144:1–8
Schwarz A-M, Hellblom F (2002) The photosynthetic light response of Halophila stipulacea growing along a depth gradient in the Gulf of Aqaba, the Red Sea. Aquat Bot 74:263–272
Sharon Y, Beer S (2008) Diurnal movements of chloroplasts in Halophila stipulacea and their effect on PAM fluorometric measurements of photosynthetic rates. Aquat Bot 88:273–276
Sharon Y, Levitan O, Spungin D, Berman-Frank I, Beer S (2011) Photoacclimation of the seagrass Halophila stipulacea to the dim irradiance at its 48-meter depth limit. Limnol Oceanogr 56:357–362
Short F, Carruthers T, Dennison W, Waycott M (2007) Global seagrass distribution and diversity: a bioregional model. J Exp Mar Biol Ecol 350:3–20
Smulders FOH, Vonk JA, Engel MS, Christianen MJA (2017) Expansion and fragment settlement of the non-native seagrass Halophila stipulacea in a Caribbean bay. Mar Biol Res 13:967–974
Steiner SCC, Willette DA (2014) Dimming sand halos on coral reefs in Dominica: new expansion corridors for the invasive seagrass Halophila stipulacea. Reef Encount 30:43–45
Steiner SCC, Willette DA (2015) The expansion of Halophila stipulacea (Hydrocharitaceae, Angiospermae) is changing the seagrass landscape in the commonwealth of Dominica, Lesser Antilles. Caribb Nat 22:1–19
Stephenson TS, Vincent LA, Allen T, Van Meerbeeck CJ, McLean N, Peterson TC, Taylor MA, Aaron-Morrison AP, Auguste T, Bernard D et al (2014) Changes in extreme temperature and precipitation in the Caribbean region, 1961–2010. Int J Climatol 34:2957–2971
Storkey J, Brooks D, Haughton A, Hawes C, Smith BM, Holland JM (2013) Using functional traits to quantify the value of plant communities to invertebrate ecosystem service providers in arable landscapes. J Ecol 101:38–46
Szmant AM, Forrester A (1996) Water column and sediment nitrogen and phosphorus distribution patterns in the Florida Keys, USA. Coral Reefs 15:21–41
Tribble GW (1981) Reef-basel herbivores and the distribution of two seagrasses (Syringodium filiforme and Thalassia testudinum) in the San Blas Islands (Western Caribbean). Mar Biol 65:277–281
van Katwijk MM, Thorhaug A, Marbà N, Orth RJ, Duarte CM, Kendrick GA, Althuizen IHJ, Balestri E, Bernard G, Cambridge ML et al (2016) Global analysis of seagrass restoration: the importance of large-scale planting. J Appl Ecol 53:567–578
van Tussenbroek BI, Cortes J, Collin R, Fonseca AC, Gayle PMH, Guzmán HM, Jácome GE, Juman R, Koltes KH, Oxenford HA et al (2014) Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse. PLoS ONE 9(3):e98377
van Tussenbroek BI, van Katwijk MM, Bouma TJ, van der Heide T, Govers LL, Leuven RSEW (2016) Non-native seagrass Halophila stipulacea forms dense mats under eutrophic conditions in the Caribbean. J Sea Res 115:1–5
Vera B, Collado-Vides L, Moreno C, van Tussenbroek BI (2014) Halophila stipulacea (Hydrocharitaceae): a recent introduction to the continental waters of Venezuela. Caribb J Sci 48:66–70
Wahbeh MI (1984) The growth and production of the leaves of the seagrass Halophila stipulacea (Forsk.) Aschers. From Aqaba Jordan. Aquat Bot 20:33–41
Weitzman JS, Zeller RB, Thomas FIM, Koseff JR (2015) The attenuation of current- and wave-driven flow within submerged multispecific vegetative canopies. Limnol Oceanogr 60:1855–1874
Welsh DT (2000) Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity. Ecol Lett 3:58–71
Willette DA, Ambrose RF (2009) The distribution and expansion of the invasive seagrass Halophila stipulacea in Dominica, West Indies, with a preliminary report from St. Lucia. Aquat Bot 91:137–142
Willette DA, Ambrose RF (2012) Effects of the invasive seagrass Halophila stipulacea on the native seagrass, Syringodium filiforme, and associated fish and epibiota communities in the Eastern Caribbean. Aquat Bot 103:74–82
Willette DA, Chalifour J, Debrot AOD, Engel MS, Miller J, Oxenford HA, Short FT, Steiner SCC, Védie F (2014) Continued expansion of the trans-Atlantic invasive marine angiosperm Halophila stipulacea in the Caribbean. Aquat Bot 112:98–102
Acknowledgements
The present paper is part of the project CIRCULATIONS (Connectivities between islands alters traveling invasive seagrasses), funded by the Leibniz- Centre for Tropical Marine Research (ZMT), Germany. Inés G. Viana was supported with a postdoctoral fellowship from Xunta de Galicia (Consellería de Cultura, Educación e Ordenación Universitaria). D. Willette thanks M. Joaquin for logistics support.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Viana, I.G., Siriwardane-de Zoysa, R., Willette, D.A. et al. Exploring how non-native seagrass species could provide essential ecosystems services: a perspective on the highly invasive seagrass Halophila stipulacea in the Caribbean Sea. Biol Invasions 21, 1461–1472 (2019). https://doi.org/10.1007/s10530-019-01924-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-019-01924-y