Our results show that water level affected the growth of A. glabra seedlings, consistent with the hypothesis of a greater biomass gain and number of leaves, as well as greater growth in height and diameter under saturated soil conditions and without salinity. These results coincide with those of various authors who have evaluated biomass gain and growth in height and diameter in seedlings of dominant tree species from swamps in the southeastern United States such as Fraxinus pennsylvanica Marshall, Nyssa aquatica, Nyssa sylvatica Marshall, Quercus michauxii Nutt., Quercus nigra L., Quercus nuttallii E.J. Palmer and Sapium sebiferum (L.) Dum. Cours., where it has been found that there is a greater gain in root and stem biomass, as well as greater growth in diameter and height when the plants are in saturated soil conditions in comparison with soil with less than five centimeters of permanent flooding (Pezeshki et al. 1989; Pezeshki 1990; Conner 1994; Conner et al. 1997, 1998; McCarron et al. 1998). Of the studies carried out in this region, only Taxodium distichum has shown a broad tolerance to flooding, with the increase in water level not having any significant effect on seedling height (Pezeshki 1990). In coastal wetlands of southeastern Australia, it was also observed that Melaleuca ericifolia Sm. grew taller and gained more biomass in wet or saturated soil treatments compared to seedlings that remained totally submerged (Salter et al. 2007). In addition, it has been documented that growth in flooded soil reduces the height of Calophyllum brasiliense Cambess. seedlings, which is a dominant species of freshwater swamps of the Amazon region in Brazil, compared to moist soil treatments; likewise, flooding also significantly reduced its root and stem biomass (Oliveira and Joly 2010). In Mexico, it has been reported that the dominant species of flooded forests that are distributed on the coast of the Gulf of Mexico, such as Pachira aquatica and Annona glabra, gain more root biomass in saturated soils compared to flooded soils (Infante-Mata et al. 2019), which coincides with the results we obtained. The reduction in root biomass may result from cell death due to the lower availability of oxygen associated with flood conditions.
Although wetland plant species have various adaptations that allow them to tolerate the stress caused by flooding and changes in soil chemistry (Pezeshki 2001; Mitsch and Gosselink 2015), most of the seedlings of these species do not grow or their growth is slower under flood conditions, because the low oxygen level of these environments is too stressful for them (Cronk and Fennesy 2001). This may indicate that these species are able to tolerate rather than require high levels of flooding to establish successfully (Infante-Mata et al. 2019). Annona glabra establishes in depressions or areas with very slow water flow, where it is not subjected to notable changes in flood level. Sexual reproduction and the establishment of pond apple are synchronized with the rainy and dry seasons, and the seedlings establish when the flood level drops and the soils remain humid (Infante-Mata and Moreno-Casasola 2005; Infante-Mata et al. 2019). Therefore, the higher growth under saturated soil conditions seems to reflect the adaptations of A. glabra to the natural conditions of the environment where it has developed.
As expected, salinity also negatively affected survival, biomass gain, leaf gain, and height and diameter growth in A. glabra seedlings. Various studies have been carried out to evaluate the response of biomass gain and growth in height or diameter to the increase in salinity of swamp tree species that are distributed in the southeastern United States such as Cephalanthus occidentalis L., Fraxinus pennsylvanica, Nyssa aquatica, Nyssa sylvatica, Quercus lyrate Walter, Quercus michauxii, Quercus nigra, Quercus nuttallii, Sapium sebiferu and Taxodium distichum (Pezeshki et al. 1989; Pezeshki 1990; Allen et al. 1994; Conner 1994; Conner et al. 1997, 1998; McCarron et al. 1998) , in the Caribbean such as Pterocarpus officinalis Jacq. (Rivera-Ocasio et al. 2007; Bompy et al. 2015), and in southeastern Australian wetlands such as Melaleuca ericifolia (Salter et al. 2007) and Eucalyptus tereticornis Sm. (Grieger et al. 2019). In these studies, it was observed that the biomass, height and diameter of the seedlings were greater in the treatments with no or low salinity compared to the high salinity treatments.
Salinity is a limiting environmental factor for the establishment of wetland plant species, because it causes physiological drought by producing a water deficit that reduces the osmotic potential of the soil (Salter et al. 2007). This represents an ecological and evolutionary barrier that prevents the germination and establishment of numerous freshwater wetland species (Wieski et al. 2010). Salinity occurs in coastal wetlands when there is the entry of marine water (Flores-Verdugo et al. 2007). In tropical or subtropical areas, the species categorized as mangroves are those that have adaptations to survive in saline soils (Cronk and Fennesy 2001). The freshwater swamps on the coastal plain of the state of Veracruz are located inland of the mangrove zone, where the sea’s influence is minimal, so the species that make up these wetlands do not have any adaptations to withstand increases in salinity. As observed in our results, survival, increases in height and diameter, and leaf and biomass gain decreased as salinity increased. However, despite the stress imposed by saline conditions, the seedlings under the Fl15‰ and Sat15‰ treatments had a slight increase in height and diameter, and a slight gain in biomass. This may be due to the fact that the seedlings in this study came from a population that is very close to a mangrove area where salinity increases periodically during the rainy season, as occurs in the species T. distichum, where the seedlings from brackish populations grow more (height and biomass) than do those from freshwater populations (Allen et al. 1994, 1997). In Veracruz, freshwater swamps with saline influence have lower species richness, and this leads to the dominance of a few salinity-tolerant species and even mixing with mangrove species (Infante-Mata 2011).
The combined increase of water and salinity levels in freshwater swamps on the floodplains of Veracruz will increase the pressure on the species that inhabit them. A. glabra seedlings were sensitive to the increase in both factors, so an increase in sea level could have a strong impact on seedling establishment in this species. However, it has been observed that the species P. aquatica (the dominant species in the other type of swamp) can survive a wide range of salinity (0.02-18 ‰) and is able to germinate in a saline solution of up to 9.2 ‰, which indicates that its germination and seedling establishment can occur in areas close to mangroves or in coexistence with them, or could occur under a scenario of rising sea level (Infante-Mata et al. 2014). Increased levels of flooding and salinity could alter the floristic composition of freshwater swamps, favoring the species that have a greater tolerance to these environmental factors (i.e., Pachira aquatica) and could damage less tolerant species (i.e., Ficus spp., Pouteria sp., Salix humboldtiana Willd., Inga vera Willd.), and even A. glabra that develop in areas with shorter and intermittent flood periods (Moreno-Casasola and Infante-Mata 2010). This could also alter the functional ecology of these ecosystems. As with A. glabra, some tree species on the Gulf of Mexico coast in the United States of America are glycophytes and are unable to tolerate high levels of salinity (Pezeshki et al. 1990). The consequences of rising sea levels could cause the deterioration or even the disappearance of freshwater swamps on the coastal plain of the Gulf of Mexico.
Despite the potentially dire consequences to freshwater swamps, with the exception of our study, there has been no work to evaluate tolerance during the seedling establishment of dominant species of tropical freshwater swamps in the face of flood conditions and increased salinity that are expected with changes in sea level, nor have scenarios been evaluated for this region of the Gulf of Mexico. It is important to mention that this study was experimental and carried out under greenhouse conditions, and thus serves as an important reference for the analysis and understanding of the response of the seedlings of this species in the field. It is necessary to continue field and greenhouse studies in the long and medium term to determine the possible impact of the rise in sea level on the regeneration of freshwater swamps. This would make it possible to propose ecological restoration strategies. Additionally, this type of information is important for developing models of the response of key ecological processes in the establishment of dominant species of freshwater swamps such as pollination, seed dispersal, productivity, germination and the establishment of seedlings. The results obtained in this study for A. glabra, as well as those mentioned for species of freshwater swamps in other regions, show that most of these species will be negatively impacted by increased flooding and salinity, which makes this type of wetland particularly vulnerable to climate change, highlighting the importance of extensive research, legislation and restoration efforts.