ARRIVAL ORDER AND AQUATIC MACROPHYTE COMMUNITY ORGANIZATION IN A TROPICAL ESTUARY
Keywords:
Spartina alterniflora, Crinum americanum, colonization, competitive exclusion, environmental gradient.Abstract
The arrival order in species colonization may be important to the communities’ organization of perennial plants along environmental gradients. In estuarine gradients, the competitive exclusion may have great importance to species zonation regardless of their arrival order. However, priority effect has also been considered, since founder species may remain in the environment even with the later arrival of species of greater competitive ability. We evaluated whether the arrival order and priority effect influence the interspecific interaction between adult individuals (early-colonizing individuals) and young individuals (later-arriving individuals) of the perennial emergent estuarine aquatic macrophytes Spartina alterniflora (S) and Crinum americanum (C). We conducted a laboratory experiment with four cultures (monocultures of early-colonizing individuals of S; monocultures of early-colonizing individuals of C; cultures of early-colonizing individuals of S with introduction of later-arriving individuals of C; and cultures of early-colonizing individuals of C with introduction of later-arriving individuals of S) and two sediment types (lower and middle estuary sediment: salinity 32 and 20, respectively). We hypothesized that, due to the priority effect, in both sediment types (i) the later-arriving species would not establish itself in adult early-colonizing vegetation and (ii) the later-arriving species would not limit the growth of the early-colonizing species. Our results corroborate our hypotheses as the later-arriving individuals of S. alterniflora and C. americanum did not grow up and establish themselves in the heterospecific cultures of early-colonizing individuals in both sediment types. Furthermore, the growth of the early-colonizing individuals was not limited by the presence of the later-arriving individuals. We conclude that the arrival order and priority effect can influence the interspecific competition, communities’ organization and spatial distribution of aquatic macrophytes in tropical estuaries.
References
Angelini, C., Altieri, A. H., Silliman, B. R., & Bertness, M. D. 2011. Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. BioScience, 61, 782–789. DOI: 10.1525/bio.2011.61.10.8
Barot, S. 2004. Mechanisms promoting plant coexistence: can all the proposed processes be reconciled? Oikos, 106, 185–192. DOI: 10.1111/j.0030-1299.2004.13038.x
Barrat-Segretain, M. H. 1996. Strategies of reproduction, dispersion, and competition in river plants: a review. Vegetatio, 123, 13–37. DOI: 10.1007/BF00044885
Bertness, M. D., & Ellison, A. M. 1987. Determinants of pattern in a New England salt marsh plant community. Ecological Monographs, 57, 129–147. DOI: 10.2307/1942621
Bickel, T. O. 2017. Processes and factors that affect regeneration and establishment of the invasive aquatic plant Cabomba caroliniana. Hydrobiologia, 788, 157–168. DOI: 10.1007/s10750-016-2995-0
Bockelmann, A. C., & Neuhaus, R. 1999. Competitive exclusion of Elymus athericus from a high-stress habitat in a European salt marsh. J. Ecol. 76: 492-402. DOI: 10.1046/j.1365-2745.1999.00368.x
Bruno, J. F., & Kennedy, C. W. 2000. Patch-size dependent habitat modification and facilitation on New England Cobble Beaches by Spartina alterniflora. Oecologia, 122, 98–108. DOI: 10.1007/PL00008841
Callaway, M. R. 1995. Positive interactions among plants. The Botanical Review, 61, 306–349. DOI: 10.1038/nature00812
Cao, H., Zhu, Z., Balke, T., Zhang, L., & Bouma, T. J. 2018. Effects of sediment disturbance regimes on Spartina seedling establishment: Implications for salt marsh creation and restoration. Limnology and Oceanography, 63, 647–659. DOI: 10.1002/lno.10657
Capers, R. S. 2003. Macrophyte colonization in a freshwater tidal wetland (Lyme, CT, USA). Aquatic Botany, 77, 325–338. DOI: 10.1016/j.aquabot.2003.08.001
Céccoli, G., Ramos, J., Pilatti, V., Dellaferrera, I., Tivano, J. C., Taleisnik, E., & Vegetti, A. C. 2015. Salt glands in the Poaceae family and their relationship to salinity tolerance. The Botanical Review, 81, 162–178. DOI: 10.1007/s12229-015-9153-7
Chadwell, T. B., & Engelhardt, K. A. M. 2008. Effects of pre-existing submersed vegetation and propagule pressure on the invasion success of Hydrilla verticillata. Journal of Applied Ecology, 45, 515–523. DOI: 10.1111/j.1365-2664.2007.01384.x
Chase, J. M. 2003. Community assembly: when should history matter? Oecologia, 136, 489–498. DOI: 10.1007/s00442-003-1311-7
Chase, J. M. 2007. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences of the United States of America, 104, 17430–17434. DOI: 10.1073/pnas.0704350104
Crain, C. M., Silliman, B. R., Bertnes, S. L., & Bertness, M. D. 2004. Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology, 85, 2539–2549. DOI: 10.1890/03-0745.
Costa, C. S., Marangoni, J. C., & Azevedo, A. M. 2003. Plant zonation in irregularly flooded salt marshes: relative importance of stress tolerance and biological interactions. Journal of Ecology, 91, 951–965. DOI: 10.1046/j.13652745.2003.00821.x
De Meester, L., Vanoverbeke, J., Kildonk, L., & Urban, M. C. 2016. Evolving perspectives on monopolization and priority effects. Trends in Ecology and Evolution, 31, 136–146. DOI: 10.1016/j.tree.2015.12.009
Dutilh, J. H. A., Oliveira, R. S., Campos-Rocha, A., Sassone, A. B., Meerow, A. W., Semir, J., Giussani, L. M., Streher, N. S., & Garcia, N. 2020. Amaryllidaceae. Flora do Brasil 2020 in construction. Jardim Botânico do Rio de Janeiro. Retrieved on March 20, 2020, from http://reflora.jbrj.gov.br/reflora/floradobrasil/FB4334
Embrapa, Empresa Brasileira de Pesquisa Agropecuária. 2015. Banco de dados climáticos do Brasil. Retrieved from http://www.bdclima.cnpm.embrapa.br/resultados/?UF=sp
Emery, N. C., Ewanchuk, P. J., & Bertness, M. D. 2001. Competition and salt-marsh plant zonation: stress tolerators may be dominant competitors. Ecology, 82, 2471–2485. DOI: 10.1890/0012-9658(2001)082[2471:CASMPZ]2.0.CO;2
Engels, J. G., & Jensen, K. 2010. Role of biotic interactions and physical factors in determining the distribution of marsh species along an estuarine salinity gradient. Oikos, 119, 679–685. DOI: 10.1111/j.1600-0706.2009.17940.x
Fried-Petersen, H. B., Araya-Ajoy, Y., Futter, M. N., & Angeler, D. G. 2020. Drivers of long-term invertebrate community stability in changing Swedish lakes. Global Change Biology, 26, 1259–1270. DOI:10.1111/gcb.14952
Fukami, T. 2015. Historical Contingency in Community Assembly: integrating niches, species pools, and priority effects. The Annual Review of Ecology, Evolution, and Systematics, 46, 1–23. DOI: 10.1146/annurev-ecolsys-110411-160340
García-Girón, J., Lindholm, M., Heino, J., Toivonen, H., & Alahuhta, J. 2021. Historical contingency via priority effects counteracts environmental change on metacommunity dynamics across decades. Limnology and Oceanography, 9999, 1–16. DOI: 10.1002/lno.11699
Ge, Y., Meng, X., Heino, J., García-Girón, J., Liu, Y. Li, Z., & Xie, Z. 2021. Stochasticity overrides deterministic processes in structuring macroinvertebrate communities in a plateau aquatic system. Ecosphere, 12(7), 1–16. DOI: 10.1002/ecs2.3675
Goldberg, D. E, & Fleetwood, L. 1987. Competitive effect and response in four annual plants. Journal of Ecology, 75, 1131–1143. DOI: 10.2307/2260318.
GraphPad Software. 2007. Prism (data analysis software system), version 5.0.
Greenwood, M. E., & Macfarlane, G. R., 2009. Effects of salinity on competitive interactions between two Juncus species. Aquatic Botany, 90, 23–29. DOI: 10.1016/j.aquabot.2008.05.001
Guo, H., Wieski, K., Lan, Z., & Pennings, S. C. 2014. Relative influence of deterministic processes on structuring marsh plant communities varies across an abiotic gradient. Oikos, 123, 173–178. DOI: 10.1890/11-0487.1.
Kardol, P., Souza, L., & Classen, A. T. 2013. Resource availability mediates the importance of priority effects in plant community assembly and ecosystem function. Oikos, 122, 84–93. DOI: 10.1111/j.1600-0706.2012.20546.x
Kim, D., Bartholdy, J., & Bartholdy, A. T. 2016. Varying patterns of vegetation dynamics across multiple levels of organization in a salt marsh of the Danish Wadden Sea. Hydrobiologia, 771, 67–81. DOI: 10.1007/s10750-015-2615-4
Körner, C., Stöcklin, J., Reuther-Thiébaud, L., & Pelaez-Riedl, S. 2008. Small differences in arrival time influence composition and productivity of plant communities. New Phytologist, 177, 698–705. DOI: 10.1111/j.1469-8137.2007.02287.x
Levine, J. M., Brewer, & J. S., Bertness, M. D. 1998. Nutrients, competition and plant zonation in a New England salt marsh. Journal of Ecology, 85, 285–292. DOI: 10.1046/j.1365-2745.1998.00253.x
Martin, J. P., Sullivan, M. J. P., Davy, A. J., Grant, A., & Mossman, H. L. 2018. Is saltmarsh restoration success constrained by matching natural environments or altered succession? A test using niche models. Journal of Applied Ecology, 55, 1207–1217. DOI: 10.1111/1365-2664.13033
Meerow, A. W., Lehmiller, D. J., & Clayton, J. R. 2003. Phylogeny and biogeography of Crinum L. (Amaryllidaceae) inferred from nuclear and limited plastid non-coding DNA sequences. Botanical Journal of the Linnean Society, 141, 349–363. DOI: 10.1046/j.1095-8339.2003.00142.x
Michelan, T., Thomaz, S. M., Bando, F. M., & Bini, L. M. 2018. Competitive effects hinder the recolonization of native species in environments densely occupied by one invasive exotic species. Frontiers in Plant Science, 9, 1–11. DOI: 10.3389/fpls.2018.01261
Monteiro, C. A. F. 1973. A dinâmica climática e as chuvas no Estado de São Paulo: estudo geográfico sob forma de atlas. São Paulo: Instituto de Geografia da Universidade de São Paulo: p. 154.
Moore, J. E., & Franklin, S. B. 2012. Water stress interacts with early arrival to influence interspecific and intraspecific priority competition: a test using a greenhouse study. Journal of Vegetation Science, 23, 647–656. DOI: 10.1111/j.1654-1103.2012.01388.x
Nunes, L. S. C., & Camargo, A. F. M. 2018. Do interspecific competition and salinity explain plant zonation in a tropical estuary? Hydrobiologia, 812, 67–77. DOI: 10.1007/s10750-016-2821-8
Nunes, L. S. C., & Camargo, A. F. M. 2017. A simple non-destructive method for estimating aboveground biomass of emergent aquatic macrophytes. Acta Limnologica Brasiliensia, 29, 1–6. DOI: 10.1590/s2179-975x6416
Nunes, L. S. C., & Camargo, A. F. M. 2020. The interspecific competition of tropical estuarine macrophytes is not density-dependent. Aquatic Botany, 164, 1–8. DOI: 10.1016/j.aquabot.2020.103233
Paradis, E., Bellavance, M. E., Fontaine, B., & Brisson, J. 2014. Interspecific competition for space between wetland plants with clonal growth. Wetlands, 34, 1003–1012. DOI: 10.1007/s13157-014-0564-8
Ribeiro, J. P., Matsumoto, R. S., Takao, L. K., Peret, A. C., & Lima, M. I. S. 2011. Spatial distribution of Crinum americanum in the tropical blind estuary: hydrologic, edaphic and biotic drivers. Environmental and Experimental Botany, 71, 287–291. DOI: 10.1016/j.envexpbot.2010.12.011
Riis, T. 2008. Dispersal and colonisation of plants in lowland streams: success rates and bottlenecks. Hydrobiologia, 596, 341–351. DOI: 10.1007/s10750-007-9107-0
Rojas-Sandoval, J., & Meléndez-Ackerman, E. 2012. Effects of an invasive grass on the demography of the Caribbean cactus Harrisia portoricensis: implications for cacti conservation. Acta Oecologica, 41, 30–38. DOI: 10.1016/j.actao.2012.04.004
Sarneel, J. M., Kardol, P., & Nilsson, C. 2016. The importance of priority effects for riparian plant community dynamics. Journal of Vegetation Science, 27, 658–667. DOI: 10.1111/jvs.12412
Schaeffer-Novelli, Y., Cintrón-Molero, G., Adaime, R. R., & Camargo, T. M. 1990. Variability of mangrove ecosystems along the Brazilian coast. Estuaries, 13, 204–218. DOI: 10.2307/1351590.
Schwarz, C., Bouma, T. J., Zhang, L. Q., Temmerman, S., Ysebaert, T., & Herman, P. M. J. 2015. Interactions between plant traits and sediment characteristics influencing species establishment and scale-dependent feedbacks in salt marsh ecosystems. Geomorphology, 250, 298–307. DOI: 10.1016/j.geomorph.2015.09.013
Shipley, B., Keddy, P. A., Moore, D. R. J., & Lemky, K. L. 1989. Regeneration and establishment strategies of emergent macrophytes. Journal of Ecology, 77, 1093–1110. DOI: 10.2307/2260825
Sikes, B. A., Hawkes, C. V., & Fukami, T. 2016. Plant and root-endophyte assembly history: interactive effects on native and exotic plants. Ecology, 97, 484–493. DOI: 10.1890/15-0635.1
StatSoft, INC., 2005. Statistica (Data Analysis Software System), Version 7.1.
Stoll, P., & Prati, D. 2001. Intraspecific aggregation alters competitive interactions in experimental plant communities. Ecology, 82, 319–327. DOI: 10.2307/2679862
Tessler, M. G., Goya, S. C., Yoshikawa, P. S., & Hurtado. S. N. 2006. Erosão de progradação do litoral brasileiro. In: D. Muehe (Ed.). Erosão de progradação do litoral brasileiro. pp. 297–346. Brasília: Ministério do Meio Ambiente.
Tognella De Rosa, M. M. P., Oliveira, R. G., Saldanha, J. H., Farias, H. C. E., Soares, M. L. G., Cunha, S. R., & Lugli, D. O. 2009. Caracterização da vegetação halófita do Saco da Fazenda. In: J. O. Branco, M. J. Lunardon-Branco, & V. R. Bellotto (Eds.). Estuário do Rio Itajaí-Açú. Santa Catarina: Caracterização ambiental e alterações antrópicas. pp. 153–170. Univali: Itajaí.
Viana, D. S., Cid, B., Figuerola, J., & Santamaría, L. 2016. Disentangling the roles of diversity resistance and priority effects in community assembly. Oecologia, 182, 865–875. DOI: 10.1007/s00442-016-3715-1
Wang, C. H., Lu, M., Yang, B., Yang, Q., Zhang, X. D., Hara, T., & Li, B. 2010. Effects of environmental gradients on the performances of four dominant plants in a Chinese saltmarsh: implications for plant zonation. Ecological Research, 25, 347–358. DOI: 10.1007/s11284-009-0662-x
Wieski, K., & Pennings, S. C. 2014. Climate drivers of Spartina alterniflora saltmarsh production in Georgia, USA. Ecosystems, 17, 473–484. DOI: 10.1007/s10021-013-9732-6
Woo, I., & Zedler, J. B. 2002. Can nutrients alone shift a sedge meadow towards dominance by the invasive Typha x Glauca? Wetlands, 22, 509–521. DOI: 10.1672/0277-5212(2002)022[0509:CNASAS]2.0.CO;2
Zee, P. C., & Fukami, T. 2018. Priority effects are weakened by a short, but no long, history of sympatric evolution. Proceedings of the Royal Society B: Biological Sciences, 285(1871), 1–8. DOI:10.1098/rspb.2017.1722
