- Email: [email protected]
closed tropical estuary
Estuarine, Coastal and Shelf Science 163 (2015) 231e234
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Short communication
The effect of competition on Bacopa monnieri zonation in an temporarily open/closed tropical estuary Jose Pedro N. Ribeiro a, *, Fernanda C.S. Tiberio b, Alexandre A. de Oliveira a a b
~o Paulo, Instituto de Bioci^ rio de Ecologia de Florestas Tropicais, Brazil Universidade de Sa encias, Departamento de Ecologia, Laborato ~o Carlos, Departamento de Bota ^nica, Brazil Universidade Federal de Sa
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 September 2014 Received in revised form 6 May 2015 Accepted 26 June 2015 Available online 30 June 2015
In this paper we investigated the role of competition to determine Bacopa monnieri L. Pennel (Plantaginaceae) zonation in a temporarily open/closed tropical estuary. In this estuary, B. monnieri occupies a given vertical zone in the saline stretch, where it forms dense monospecific stands, but is absent elsewhere. We transplanted turfs to areas outside of their natural occurrence in the estuary, both in the presence and absence of competition: a higher-elevation zone, a lower-elevation zone and a non-saline region. Turfs transplanted between naturally occurring stands served as controls. Turfs transplanted to the lower zone either died or became much smaller. As there was no competition under this condition, we conclude that the absence of this species from this zone is due to abiotic conditions, likely light limitation imposed by the turbid water column. Turfs transplanted to the higher zone under competition died; however, in the absence of competition, they survived. Turfs transplanted to the non-saline zone died, regardless of the presence or absence of competition, indicating an abiotic restraint. Our results indicate that the absence of B. monnieri from higher elevations is related to competitive displacement, whereas its absence from lower elevations and from non-saline areas is related to abiotic drivers. © 2015 Published by Elsevier Ltd.
Keywords: Biotic interaction Coastal environment Flooding Organic matter Salt
1. Introduction Plant competition is one of the most important factors determining plant zonation, and competitive interactions play a major role in ecosystem structure and function (Peyre et al., 2001; Zhang, 2010). As different species vary in their responses to abiotic drivers, the environment modulates biotic interactions. Therefore, plant competition is influenced by local abiotic conditions, and the outcome species (and consequently, the plant assemblages) can vary extensively along an abiotic gradient (Costa et al., 2003; Emery et al., 2001; Ribeiro et al., 2011a). Estuaries are favourable systems for investigating the relationships between competition and abiotic conditions (Emery et al., 2001) because they are clearly delimited (Vannucci, 2001) and have obvious gradients. In these environments, competitive species are expected to occupy the less restrictive zones, displacing subordinate species (Crain et al., 2004; Grime, 1977). Experiments where competition is suppressed have demonstrated that species characteristic of the saline region can
* Corresponding author. E-mail address: [email protected] (J.P.N. Ribeiro). http://dx.doi.org/10.1016/j.ecss.2015.06.029 0272-7714/© 2015 Published by Elsevier Ltd.
typically survive upstream but that freshwater species often die when transplanted to the saline zone, regardless of the level of competition (Bertness, 1991; Crain et al., 2004; Pennings et al., 2005). These findings suggest that competitive interactions distant from tidal influences are more intense, whereas near the estuary mouth, abiotic drivers act directly on species distributions (Davy et al., 2011; Pennings and Callaway, 1992). Bacopa monnieri L. Pennel (Plantaginaceae) is a small herb widely distributed in the tropics and subtropics, living within or adjacent to water bodies. It is also commonly used for freshwater aquariums, in which it can live permanently submerged. In Massaguaçu River Estuary (23 370 2000 S and 45 2102500 W), a tropical, temporally open/closed estuary (see Ribeiro et al. (2013) for breaching cycles description and full species inventory; Ribeiro et al. (2011b)) where we performed the present work, B. monnieri forms large monospecific stands near the bar but is absent upstream. Vertically, it occupies deeper (but not the deepest) zones. As this species can live either completely or partially submerged in freshwater or live unsubmerged, we hypothesized that its absence from the shallower, deeper and freshwater zones is due to competitive displacement. To test this hypothesis, we transplanted this species to these areas and artificially removed competition.
232
J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
2. Material and methods We selected three monospecific stands of B. monnieri from which we randomly collected 72 cylindrical turfs (15-cm diameter, 25 cm deep) containing B. monnieri and sediment using a PVC pipe. We randomly transplanted 12 of these turfs, divided in three blocks of four (Fig. 1F), to each of the following environments along a vertical gradient: 1) Forest e a high-zone area shaded by dense canopy, flooded only at very high water levels; 2) Forest Pots e similar flooding condition as Forest, but with the turfs placed in pots outside the canopy and 3) Deep e a zone just below the natural occurrence of B. monnieri. In the Deep zone, we did not suppress competition, as it already have no vegetation. Along the horizontal salinity gradient, we transplanted turfs to the freshwater zone, maintaining the same elevation as the original stands, so that transplants and the original stand experienced the same flooding conditions. In the freshwater zone transplants were made either 4) with a crown, where competitors were removed, or 5) without a crown. 6) Control e turfs transplanted among the monospecific stands of B. monnieri to examine possible effects of the transplantation. We additionally established 12 points in the stands as References, where we monitored not transplanted individuals of B. monnieri. We monitored turf performance by measuring the cover area (cm2). As an open sandbar was required to record these measurements, measurement intervals were irregular, occurring at months 0, 3, 5, 8.5 and 13.5 (from September 2011 to October 2012). Control and Reference turfs and adjacent vegetation became indiscernible during the experiment. A similar problem was encountered with the pots when the plants grew to occupy all of the available area (details in Results and discussion). Therefore, when the cover area exceeded the pot area (452 cm2), we stopped measuring cover area and simply monitored turf presence/absence. For analysis purposes, 452 cm2 was assigned to these turfs. Between months 5 and 8.5, the plants experienced herbivory from ants. Several Forest Pot turfs died or were severely injured. Thus, we performed formal statistical analysis up to month 5 and discuss the subsequent data without a formal test. We used a linear mixed model fit by maximum likelihood to estimate B. monnieri performance in response to competition, salinity and flooding. The full
model included these three drivers and the interaction between flooding and salinity. We included block as random effect. To determine the minimal adequate model, we used the process of model simplification based on the model deviance values (Crawley, 2007). 3. Results and discussion After transplantation, the cover areas of the Control and Reference turfs increased by similar extents, and after five months, they were no longer discernable from one another (Fig. 1a). Turfs transplanted to Forest Pots grew quickly, and most pots were completely covered upon the first measurement (Fig. 1c). In contrast, turfs transplanted to Forest decreased in size, becoming considerably smaller or dying after 5 months (Fig. 1b). At the beginning of the experiment, the average turf covering area decreased in Deep zones, although some turfs had increased in area (Fig. 1). Along the horizontal saline gradient, regardless of competition level, all turfs were dead upon the first measurement (Fig. 2). The selected model included salinity, which was positively related to covering area. It also included competition and the interaction of flooding and salinity, which were both negatively related with turf covering area. Bacopa monnieri has low nutritional requirements (Fang et al., 2007), and soil under the canopy is much richer than the poor sandy soil B. monnieri is able to live. Therefore, below-ground competition was unlikely to be an important factor. In contrast, shading is an important limiting factor of submerged macrophytes (Phillips et al., 1978). Although an experiment specifically designed to separate below- and above-ground competition would be informative, it is likely that the competitive displacement experienced by B. monnieri in Forest was due to light limitation. The performance of turfs in Forest Pots in the first month of the experiment was equivalent to that of Control. Furthermore, plants in the pots flowered (Fig. 1c). Plants in Forest Pots and Control experienced very different flooding cycles; however, B. monnieri can survive in both conditions. The selected model did not include flooding but related competition with a large reduction in turf covering area. Commonly, plants from abiotic restrictive zones perform better in less restrictive zones when their neighbours are excluded. Although competition is the key influence on
Fig. 1. Bacopa monieri transplants: A) reference, B) forest, C) forest pots, with flowers, D) detail of the ant attack, E) deeper zones and. F) control.
J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
233
Fig. 2. Boxplot with Bacopa monieri transplants.
B. monnieri occurrence, it is likely that it would perform better when less flooded in the absence of competitors. Thus, frequent flooding is an ecological refuge rather than a physiological demand. Soil salinity is partially dependent upon flooding, and soil at higher elevations has lower salinity on average. Thus, the transplants along vertical gradient experienced changes in soil salinity. The selected model detected this interaction, which was related to a decrease in turf covering area. At the Deep zone, turfs showed no clear growth pattern, although the average turf covering area decreased. As biotic interactions are almost non-existent in Deep zones and as B. monnieri can survive in permanently flooded areas, it is likely that the decrease in covering area is due to the light limitation imposed by the high-turbidity water column rather than the flooding itself. From month 8.5, the cover area of Deep turfs decreased, and by month 13.5, the turfs had either become smaller or died. Salt can be a physiological or an ecological requirement (Wang et al., 2011). The selected model related salinity to a slight increase in turf covering area. When transplanted to the freshwater zone, turfs died, regardless of the presence of competition. This result does not corroborate our hypotheses, and we conclude that some abiotic condition is preventing the occurrence of B. monnieri in the freshwater zone. However, as B. monnieri can survive without salinity in other areas (Horník et al., 2008; Pierce et al., 2009; Rolon et al., 2012), we posit that this abiotic condition is not directly related to the absence of salt, but varies with it. Nonetheless, we noted that turfs in the non-saline zone were buried in organic matter. This pattern might reflect greater productivity upstream or reduced water flow that allows organic matter to accumulate. It is likely that turf mortality is related to the presence of organic
matter, although organic matter may be more a function of competition than of abiotic conditions. Thus, we conclude that the distribution of B. monnieri is biotically driven in the upper part of the vertical flooding gradient and by abiotic drivers in both the lower part of the vertical flooding gradient and the freshwater zone. We never observed herbivory on B. monnieri in its natural zone of occurrence. However, the plants in the pots were severely injured by ant herbivory. Ant herbivory was also observed in another experiment conducted at the study site, in which Crinum americanum L. were preyed upon when transplanted out of the water. Both B. monnieri and C. americanum are soft-tissue plants with no physical defence mechanisms but with strong allelopathic properties (Takao et al., 2011), suggesting they rely on chemical defences to avoid herbivory. This interpretation is consistent with the findings of Morrison and Hay (2011) that indicate high investment in chemical defences among tropical macrophytes. This strategy, however, appears to be ineffective against terrestrial herbivores. This hypothesis has yet to be tested. Acknowledgements ~o de Amparo a We would like to acknowledge the Fundaça ~o Paulo (FAPESP) for funding this research Pesquisa do Estado de Sa (process number: 2011/02131-0) and the Conselho Nacional de ^ntífico (CNPq) for a scholarship awarded to Desenvolvimento Cie the second author. We also would like to thank Renata Balsamo Dias, Ricardo Santos Duran and Valdemir Goncalvez Pereira for field assistance.
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J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
References Bertness, M.D., 1991. Interspecific interactions among high marsh perennials in a New England salt marsh. Ecology 72, 138e148. Costa, C.S.B., Marangoni, J.C., Azevedo, A.M.G., 2003. Plant zonation in a irregular flooded salt marshes: relative importance of stress tolerance and biological interactions. J. Ecol. 91, 951e965. Crain, C.M., Silliman, B.R., Bertness, S.L., Bertness, M.D., 2004. Physical and biotic drivers of plant distribution across estuarune salinity gradients. Ecology 85, 2539e2549. Crawley, M.J., 2007. The R Book. John Wiley & Sons, West Sussex, England. Davy, A.J., Brown, M.J.H., Mossman, H.L., Grant, A., 2011. Colonization of a newly developing salt marsh: disentangling independent effects of elevation and redox potential on halophytes. J. Ecol. 99, 1350e1357. Emery, N.C., Ewanchuk, P.J., Bertness, M.D., 2001. Competition and salt-mash plant zonation: stress tolerantors may be dominant competitors. Ecology 82, 2471e2485. Fang, Y.Y., Babourina, O., Rengel, Z., Yang, X.E., Pu, P.M., 2007. Spatial distribution of ammonium and nitrate fluxes along roots of wetland plants. Plant Sci. 173, 240e246. Grime, J.P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169e1194. Horník, M., Pipíska, M., Augustín, J., 2008. Bioaccumulation of 137Cs and 60Co in freshwater plants. Nova Biotechnol. 8, 55e63. Morrison, W.E., Hay, M.E., 2011. Are lower-latitude plants better defended? Palatability of freshwater macrophytes. Ecology 93, 65e74. Pennings, S.C., Callaway, R.M., 1992. Salt marsh plant zonation: the relative importance of competition and physical factors. Ecology 73, 681e690. Pennings, S.C., Grant, M.-B., Bertness, M.D., 2005. Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J. Ecol.
93, 159e167. Peyre, M.K.G.L., Grace, J.B., Hahn, E., Mendelssohn, I.A., 2001. The importance of competition in regulating plant species abundance along a salinity gradient. Ecology 82, 62e69. Phillips, G.L., Eminson, D.F., Moss, B., 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwater. Aquat. Bot. 4, 103e126. Pierce, S.C., Pezeshki, S.R., Larsen, D., Moore, M.T., 2009. Hydrology and speciesspecific effects of Bacopa monnieri and Leersia oryzoides on soil and water chemistry. Ecohydrology 2, 279e286. Ribeiro, J.P.N., Matsumoto, R.S., Takao, L.K., Peret, A.C., Lima, M.I.S., 2011a. Spatial distribution of Crinum americanum L. in tropical blind estuary: hydrologic, edaphic and biotic drivers. Environ. Exp. Bot. 71, 287e291. ^ Lima, M.I.S., 2013. The effects of artificial sandbar Ribeiro, J.P.N., Saggio, A., breaching on the macrophyte communities of an intermittently open estuary. Estuar. Coast. Shelf Sci. 121e122, 33e39. Ribeiro, J.P.N., Takao, L.K., Matsumoto, R.S., Urbanetz, C., Lima, M.I.S., 2011b. Plantae, aquatic, amphibian and marginal species, massaguaçu river estuary, Car~o Paulo, Brazil. Check List 7, 133e138. aguatatuba, Sa Rolon, A.S., Rocha, O., Maltchik, L., 2012. Do effects of landscape factors on coastal pond macrophyte communities depend on species traits? Aquat. Bot. 103, 115e121. fitas Takao, L.K., Ribeiro, J.P.N., Lima, M.I.S., 2011. Potential alelop atico de macro ticas de um estua rio cego. Acta Bot. Bras. 25, 324e330. aqua Vannucci, M., 2001. What is so special about mangroves? Braz. J. Biol. 61, 599e603. Wang, W., Yan, Z., You, S., Zhang, Y., Chen, L., Lin, G., 2011. Mangroves: obligate or facultative halophytes? A review. Trees Struct. Funct. 25, 953e963. Zhang, X.F., 2010. Competitive interaction effects of Hydrilla verticillata and Vallisneria natans on phosphorus concentrations in water. Procedia Environ. Sci. 2, 636e642.
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Short communication
The effect of competition on Bacopa monnieri zonation in an temporarily open/closed tropical estuary Jose Pedro N. Ribeiro a, *, Fernanda C.S. Tiberio b, Alexandre A. de Oliveira a a b
~o Paulo, Instituto de Bioci^ rio de Ecologia de Florestas Tropicais, Brazil Universidade de Sa encias, Departamento de Ecologia, Laborato ~o Carlos, Departamento de Bota ^nica, Brazil Universidade Federal de Sa
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 September 2014 Received in revised form 6 May 2015 Accepted 26 June 2015 Available online 30 June 2015
In this paper we investigated the role of competition to determine Bacopa monnieri L. Pennel (Plantaginaceae) zonation in a temporarily open/closed tropical estuary. In this estuary, B. monnieri occupies a given vertical zone in the saline stretch, where it forms dense monospecific stands, but is absent elsewhere. We transplanted turfs to areas outside of their natural occurrence in the estuary, both in the presence and absence of competition: a higher-elevation zone, a lower-elevation zone and a non-saline region. Turfs transplanted between naturally occurring stands served as controls. Turfs transplanted to the lower zone either died or became much smaller. As there was no competition under this condition, we conclude that the absence of this species from this zone is due to abiotic conditions, likely light limitation imposed by the turbid water column. Turfs transplanted to the higher zone under competition died; however, in the absence of competition, they survived. Turfs transplanted to the non-saline zone died, regardless of the presence or absence of competition, indicating an abiotic restraint. Our results indicate that the absence of B. monnieri from higher elevations is related to competitive displacement, whereas its absence from lower elevations and from non-saline areas is related to abiotic drivers. © 2015 Published by Elsevier Ltd.
Keywords: Biotic interaction Coastal environment Flooding Organic matter Salt
1. Introduction Plant competition is one of the most important factors determining plant zonation, and competitive interactions play a major role in ecosystem structure and function (Peyre et al., 2001; Zhang, 2010). As different species vary in their responses to abiotic drivers, the environment modulates biotic interactions. Therefore, plant competition is influenced by local abiotic conditions, and the outcome species (and consequently, the plant assemblages) can vary extensively along an abiotic gradient (Costa et al., 2003; Emery et al., 2001; Ribeiro et al., 2011a). Estuaries are favourable systems for investigating the relationships between competition and abiotic conditions (Emery et al., 2001) because they are clearly delimited (Vannucci, 2001) and have obvious gradients. In these environments, competitive species are expected to occupy the less restrictive zones, displacing subordinate species (Crain et al., 2004; Grime, 1977). Experiments where competition is suppressed have demonstrated that species characteristic of the saline region can
* Corresponding author. E-mail address: [email protected] (J.P.N. Ribeiro). http://dx.doi.org/10.1016/j.ecss.2015.06.029 0272-7714/© 2015 Published by Elsevier Ltd.
typically survive upstream but that freshwater species often die when transplanted to the saline zone, regardless of the level of competition (Bertness, 1991; Crain et al., 2004; Pennings et al., 2005). These findings suggest that competitive interactions distant from tidal influences are more intense, whereas near the estuary mouth, abiotic drivers act directly on species distributions (Davy et al., 2011; Pennings and Callaway, 1992). Bacopa monnieri L. Pennel (Plantaginaceae) is a small herb widely distributed in the tropics and subtropics, living within or adjacent to water bodies. It is also commonly used for freshwater aquariums, in which it can live permanently submerged. In Massaguaçu River Estuary (23 370 2000 S and 45 2102500 W), a tropical, temporally open/closed estuary (see Ribeiro et al. (2013) for breaching cycles description and full species inventory; Ribeiro et al. (2011b)) where we performed the present work, B. monnieri forms large monospecific stands near the bar but is absent upstream. Vertically, it occupies deeper (but not the deepest) zones. As this species can live either completely or partially submerged in freshwater or live unsubmerged, we hypothesized that its absence from the shallower, deeper and freshwater zones is due to competitive displacement. To test this hypothesis, we transplanted this species to these areas and artificially removed competition.
232
J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
2. Material and methods We selected three monospecific stands of B. monnieri from which we randomly collected 72 cylindrical turfs (15-cm diameter, 25 cm deep) containing B. monnieri and sediment using a PVC pipe. We randomly transplanted 12 of these turfs, divided in three blocks of four (Fig. 1F), to each of the following environments along a vertical gradient: 1) Forest e a high-zone area shaded by dense canopy, flooded only at very high water levels; 2) Forest Pots e similar flooding condition as Forest, but with the turfs placed in pots outside the canopy and 3) Deep e a zone just below the natural occurrence of B. monnieri. In the Deep zone, we did not suppress competition, as it already have no vegetation. Along the horizontal salinity gradient, we transplanted turfs to the freshwater zone, maintaining the same elevation as the original stands, so that transplants and the original stand experienced the same flooding conditions. In the freshwater zone transplants were made either 4) with a crown, where competitors were removed, or 5) without a crown. 6) Control e turfs transplanted among the monospecific stands of B. monnieri to examine possible effects of the transplantation. We additionally established 12 points in the stands as References, where we monitored not transplanted individuals of B. monnieri. We monitored turf performance by measuring the cover area (cm2). As an open sandbar was required to record these measurements, measurement intervals were irregular, occurring at months 0, 3, 5, 8.5 and 13.5 (from September 2011 to October 2012). Control and Reference turfs and adjacent vegetation became indiscernible during the experiment. A similar problem was encountered with the pots when the plants grew to occupy all of the available area (details in Results and discussion). Therefore, when the cover area exceeded the pot area (452 cm2), we stopped measuring cover area and simply monitored turf presence/absence. For analysis purposes, 452 cm2 was assigned to these turfs. Between months 5 and 8.5, the plants experienced herbivory from ants. Several Forest Pot turfs died or were severely injured. Thus, we performed formal statistical analysis up to month 5 and discuss the subsequent data without a formal test. We used a linear mixed model fit by maximum likelihood to estimate B. monnieri performance in response to competition, salinity and flooding. The full
model included these three drivers and the interaction between flooding and salinity. We included block as random effect. To determine the minimal adequate model, we used the process of model simplification based on the model deviance values (Crawley, 2007). 3. Results and discussion After transplantation, the cover areas of the Control and Reference turfs increased by similar extents, and after five months, they were no longer discernable from one another (Fig. 1a). Turfs transplanted to Forest Pots grew quickly, and most pots were completely covered upon the first measurement (Fig. 1c). In contrast, turfs transplanted to Forest decreased in size, becoming considerably smaller or dying after 5 months (Fig. 1b). At the beginning of the experiment, the average turf covering area decreased in Deep zones, although some turfs had increased in area (Fig. 1). Along the horizontal saline gradient, regardless of competition level, all turfs were dead upon the first measurement (Fig. 2). The selected model included salinity, which was positively related to covering area. It also included competition and the interaction of flooding and salinity, which were both negatively related with turf covering area. Bacopa monnieri has low nutritional requirements (Fang et al., 2007), and soil under the canopy is much richer than the poor sandy soil B. monnieri is able to live. Therefore, below-ground competition was unlikely to be an important factor. In contrast, shading is an important limiting factor of submerged macrophytes (Phillips et al., 1978). Although an experiment specifically designed to separate below- and above-ground competition would be informative, it is likely that the competitive displacement experienced by B. monnieri in Forest was due to light limitation. The performance of turfs in Forest Pots in the first month of the experiment was equivalent to that of Control. Furthermore, plants in the pots flowered (Fig. 1c). Plants in Forest Pots and Control experienced very different flooding cycles; however, B. monnieri can survive in both conditions. The selected model did not include flooding but related competition with a large reduction in turf covering area. Commonly, plants from abiotic restrictive zones perform better in less restrictive zones when their neighbours are excluded. Although competition is the key influence on
Fig. 1. Bacopa monieri transplants: A) reference, B) forest, C) forest pots, with flowers, D) detail of the ant attack, E) deeper zones and. F) control.
J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
233
Fig. 2. Boxplot with Bacopa monieri transplants.
B. monnieri occurrence, it is likely that it would perform better when less flooded in the absence of competitors. Thus, frequent flooding is an ecological refuge rather than a physiological demand. Soil salinity is partially dependent upon flooding, and soil at higher elevations has lower salinity on average. Thus, the transplants along vertical gradient experienced changes in soil salinity. The selected model detected this interaction, which was related to a decrease in turf covering area. At the Deep zone, turfs showed no clear growth pattern, although the average turf covering area decreased. As biotic interactions are almost non-existent in Deep zones and as B. monnieri can survive in permanently flooded areas, it is likely that the decrease in covering area is due to the light limitation imposed by the high-turbidity water column rather than the flooding itself. From month 8.5, the cover area of Deep turfs decreased, and by month 13.5, the turfs had either become smaller or died. Salt can be a physiological or an ecological requirement (Wang et al., 2011). The selected model related salinity to a slight increase in turf covering area. When transplanted to the freshwater zone, turfs died, regardless of the presence of competition. This result does not corroborate our hypotheses, and we conclude that some abiotic condition is preventing the occurrence of B. monnieri in the freshwater zone. However, as B. monnieri can survive without salinity in other areas (Horník et al., 2008; Pierce et al., 2009; Rolon et al., 2012), we posit that this abiotic condition is not directly related to the absence of salt, but varies with it. Nonetheless, we noted that turfs in the non-saline zone were buried in organic matter. This pattern might reflect greater productivity upstream or reduced water flow that allows organic matter to accumulate. It is likely that turf mortality is related to the presence of organic
matter, although organic matter may be more a function of competition than of abiotic conditions. Thus, we conclude that the distribution of B. monnieri is biotically driven in the upper part of the vertical flooding gradient and by abiotic drivers in both the lower part of the vertical flooding gradient and the freshwater zone. We never observed herbivory on B. monnieri in its natural zone of occurrence. However, the plants in the pots were severely injured by ant herbivory. Ant herbivory was also observed in another experiment conducted at the study site, in which Crinum americanum L. were preyed upon when transplanted out of the water. Both B. monnieri and C. americanum are soft-tissue plants with no physical defence mechanisms but with strong allelopathic properties (Takao et al., 2011), suggesting they rely on chemical defences to avoid herbivory. This interpretation is consistent with the findings of Morrison and Hay (2011) that indicate high investment in chemical defences among tropical macrophytes. This strategy, however, appears to be ineffective against terrestrial herbivores. This hypothesis has yet to be tested. Acknowledgements ~o de Amparo a We would like to acknowledge the Fundaça ~o Paulo (FAPESP) for funding this research Pesquisa do Estado de Sa (process number: 2011/02131-0) and the Conselho Nacional de ^ntífico (CNPq) for a scholarship awarded to Desenvolvimento Cie the second author. We also would like to thank Renata Balsamo Dias, Ricardo Santos Duran and Valdemir Goncalvez Pereira for field assistance.
234
J.P.N. Ribeiro et al. / Estuarine, Coastal and Shelf Science 163 (2015) 231e234
References Bertness, M.D., 1991. Interspecific interactions among high marsh perennials in a New England salt marsh. Ecology 72, 138e148. Costa, C.S.B., Marangoni, J.C., Azevedo, A.M.G., 2003. Plant zonation in a irregular flooded salt marshes: relative importance of stress tolerance and biological interactions. J. Ecol. 91, 951e965. Crain, C.M., Silliman, B.R., Bertness, S.L., Bertness, M.D., 2004. Physical and biotic drivers of plant distribution across estuarune salinity gradients. Ecology 85, 2539e2549. Crawley, M.J., 2007. The R Book. John Wiley & Sons, West Sussex, England. Davy, A.J., Brown, M.J.H., Mossman, H.L., Grant, A., 2011. Colonization of a newly developing salt marsh: disentangling independent effects of elevation and redox potential on halophytes. J. Ecol. 99, 1350e1357. Emery, N.C., Ewanchuk, P.J., Bertness, M.D., 2001. Competition and salt-mash plant zonation: stress tolerantors may be dominant competitors. Ecology 82, 2471e2485. Fang, Y.Y., Babourina, O., Rengel, Z., Yang, X.E., Pu, P.M., 2007. Spatial distribution of ammonium and nitrate fluxes along roots of wetland plants. Plant Sci. 173, 240e246. Grime, J.P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111, 1169e1194. Horník, M., Pipíska, M., Augustín, J., 2008. Bioaccumulation of 137Cs and 60Co in freshwater plants. Nova Biotechnol. 8, 55e63. Morrison, W.E., Hay, M.E., 2011. Are lower-latitude plants better defended? Palatability of freshwater macrophytes. Ecology 93, 65e74. Pennings, S.C., Callaway, R.M., 1992. Salt marsh plant zonation: the relative importance of competition and physical factors. Ecology 73, 681e690. Pennings, S.C., Grant, M.-B., Bertness, M.D., 2005. Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J. Ecol.
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