Ammonium uptake plasticity and allocation trade-offs may shape invasion potential in Caribbean seagrasses

Ammonium uptake plasticity and allocation trade-offs may shape invasion potential in Caribbean seagrasses | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 8 January 2026 V1 Latest version Share on Ammonium uptake plasticity and allocation trade-offs may shape invasion potential in Caribbean seagrasses Authors : Fee Smulders 0000-0003-4124-8355 [email protected] , Divyashri Varadharajan , Marjolijn Christianen , and Arie Vonk Authors Info & Affiliations https://doi.org/10.22541/au.176786483.34297953/v1 141 views 86 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract Nutrient uptake traits can shape plant competition, yet nutrient acquisition and internal allocation strategies remain poorly resolved for invasive seagrasses, limiting predictions of species responses to coastal nutrient enrichment. Over the past two decades, the invasive seagrass Halophila stipulacea has rapidly colonized large areas of the Mediterranean and Caribbean, occasionally displacing native species. Competition for inorganic nitrogen, particularly ammonium, may play a key role role in determining future meadow composition and functioning. Using a novel split-chamber incubation system, we compared leaf and root ammonium ( 15 NH 4 + ) uptake kinetics and internal nitrogen transfer among three native Caribbean seagrasses ( Thalassia testudinum, Halodule wrightii, Syringodium filiforme ) and the invasive H. stipulacea . We further synthesized available data on seagrass ammonium uptake and transfer parameters to place our findings in a broader context. Across all species, leaf uptake dominated and was nearly an order of magnitude higher than root uptake. Native species exhibited high root uptake affinity and balanced allocation, consistent with nutrient-conservative strategies in oligotrophic enivronments. In contrast, H. stipulacea showed lower root uptake but exceptionally high maximum leaf uptake rates and strong root-to-leaf transfer at elevated ammonium, indicating opportunistic aboveground allocation under nutrient pulses. Some species displayed non-saturating uptake kinetics, suggesting uptake capacity may be underestimated under eutrophic conditions. Our synthesis revealed high inter- and intraspecific variability and showed that 80% of seagrass species lack kinetic parameters, highlighting major mechanistic knowledge gaps in this foundational plant group. Native Caribbean seagrasses are likely competitively favoured under low to moderate ammonium concentrations, whereas H. stipulacea may gain a context-dependent advantage under nutrient enrichment. These findings illustrate how trade-offs between nutrient-use efficiency and flexibility shape invasion potential. Closing global data gaps, monitoring nutrient levels and thereby identifying mechanistic thresholds is essential for predicting future seagrass species dominance and ecosystem functioning in increasingly eutrophic seagrass meadows. Title Ammonium uptake plasticity and allocation trade-offs may shape invasion potential in Caribbean seagrasses Abstract Nutrient uptake traits can shape plant competition, yet nutrient acquisition and internal allocation strategies remain poorly resolved for invasive seagrasses, limiting predictions of species responses to coastal nutrient enrichment. Over the past two decades, the invasive seagrass Halophila stipulacea has rapidly colonized large areas of the Caribbean, occasionally displacing native species. Competition for inorganic nitrogen, particularly ammonium, may play a key role role in determining future meadow composition and functioning. Using a novel split-chamber incubation system, we compared leaf and root ammonium ( 15 NH 4 + ) uptake kinetics and internal nitrogen transfer among three native Caribbean seagrasses ( Thalassia testudinum, Halodule wrightii, Syringodium filiforme ) and the invasive H. stipulacea. We further synthesized available data on seagrass ammonium uptake and transfer parameters to place our findings in a broader context. Across all species, leaf uptake dominated and was nearly an order of magnitude higher than root uptake. Native species exhibited high root uptake affinity and stronger bidirectional transfer, consistent with nutrient-conservative strategies in oligotrophic enivronments. In contrast, H. stipulacea showed lower root uptake but exceptionally high maximum leaf uptake rates and strong root-to-leaf transfer at elevated ammonium, indicating opportunistic aboveground allocation under nutrient pulses. Some species displayed non-saturating uptake kinetics, suggesting uptake capacity may be underestimated under eutrophic conditions. Our synthesis revealed high inter- and intraspecific variability and showed that 80% of seagrass species lack kinetic parameters, highlighting major mechanistic knowledge gaps in this foundational plant group. Native Caribbean seagrasses are likely competitively favoured under low to moderate ammonium concentrations, whereas H. stipulacea may gain a context-dependent advantage under nutrient enrichment. These findings illustrate how trade-offs between nutrient-use efficiency and flexibility shape invasion potential. Closing global data gaps, monitoring nutrient levels and thereby identifying mechanistic thresholds is essential for predicting future seagrass species dominance and ecosystem functioning in increasingly eutrophic seagrass meadows. Keywords Angiosperms, eutrophication, Halophila stipulacea, i nvasion ecology, nitrogen translocation, nutrient uptake, Thalassia testudinum 1. Introduction Seagrasses are marine angiosperms that form one of the most productive autotroph communities in the world (Unsworth et al. , 2022; Krause et al. , 2025). This is partly because seagrasses are efficient at taking up low concentrations of nutrients both through their leaf and root systems (Romero et al. , 2006). Through their efficient nutrient acquisition, they form productive ecosystems in oligotrophic areas, further stimulating the foodweb and providing essential ecosystem services (Nordlund et al. , 2016). However, seagrass meadows are declining worldwide (Waycott et al. , 2009; Dunic et al. , 2021), partly due to deteriorating water quality caused by nutrient influxes. Elevated nutrient concentrations in the water can favor the growth of fast-growing algae outcompeting seagrasses for water-column resources or inhibiting light (Tomasko & Lapointe, 1991; McGlathery et al. , 2007; Maxwell et al. , 2017), as well as potentially favor fast-growing native pioneer or invasive macrophytes over native climax species. Ammonium, the primary bioavailable form of inorganic nitrogen for seagrasses, originates mainly from sediment porewater under pristine conditions (Fourqurean et al., 1992; Burkholder et al., 2007), but additional inputs from wastewater can elevate its concentration in the water column (Fourqurean et al. , 1992; den Haan et al. , 2016; Vieira et al. , 2024). Both seagrass leaves and roots prefer ammonium over nitrate, as assimilation of the latter is energetically more expensive, with higher uptake rates for leaves compared to roots (Vonk et al. , 2008; Alexandre et al. , 2011a; Viana et al. , 2019). Therefore, understanding ammonium uptake kinetics across species is essential, yet current data remain fragmented. In pristine conditions, over time, climax species, like Thalassia spp., have high nutrient affinity and can assimilate nutrients to concentrations below the minimum requirement of early successional pioneer species (van Tussenbroek et al. , 2006), progressing seagrass meadows to a climax state. However, as nutrient inputs into seagrass meadows increase, climax species may lose this competitive advantage to pioneer species, either native or exotic, that have high maximum nutrient uptake rates and can therefore exploit nutrient pulses (Fourqurean et al. , 1995). It is unknown if the same mechanim applies to successful exotic seagrasses. Studying ammonium uptake kinetics of of both native and exotic seagrasses with different growing strategies is therefore vital for understanding their competitive responses to nutrient enrichment. This helps to assess if future increases in nutrient loads may result in reverse succession with cascading effects on ecosystem functioning (O’Brien et al. , 2018; Manhães et al. , 2022). In the Caribbean, the pioneer seagrass Halophila stipulacea, native to the Red Sea and Indo-Pacific, has been expanding its range since its first detection in 2004 (Winters et al. , 2020). Several studies have characterised this species as invasive due to its rapid proliferation and apparent replacement of native seagrass species such as Thalassia testudinum, Halodule wrightii, and Syringodium filiforme (Steiner & Willette, 2015; Smulders et al. , 2017; Scheibling et al. , 2018). Although direct evidence of H. stipulacea outcompeting native seagrass for nutrients or light remains limited (Winters et al. , 2020), indirect evidence suggest potential competitive advantanges, such as dense, monospecific invasive meadows in areas with high sediment nitrogen contents (van Tussenbroek et al. , 2016). Nutrient uptake kinetics, often quantified using the Michaelis-Menten parameters maximum uptake rate (V max ) and half saturation constant (K m ), show considerable variability for among native species such as T. testudinum in both leaves and roots (Lee & Dunton, 1999) , while data for H. stipulacea are currently available only from its invasive Mediterranean populations (Alexandre et al. , 2014) and have never been compared directly to native species within one experiment. Because Caribbean populations of H. stipulacea exhibit superior growth traits compared to both native and Mediterranean populations (Winters et al. , 2023) we consider H. stipulacea an invasive species in the Carribean context for the purposes of this study. Understanding its nutrient uptake dynamics in comparison to native seagrasses is therefore essential to predict competitive outcomes. To assess the ammonium uptake kinetics in Caribbean seagrasses, we asked three key questions: (i) How do ammonium uptake kinetics differ between native and invasive species across plant structures (leaves vs. roots)? (ii) How does nitrogen transfer between roots and leaves vary among native and invasive species? (iii) How do the ammonium uptake kinetics and transfer data compare to those previously reported in literature? We hypothesize that native climax species would exhibit higher ammonium affinity (α, V max /K m ) but lower maximum uptake rates than the invasive H. stipulacea . We also expect leaf uptake rates to exceed root uptake across species. To test these hypotheses, we used a split-chamber experimental setup that allowed separate quantification of above- and belowground nutrient uptake using 15 N-labeled ammonium as a tracer under controlled laboratory conditions. Finally, we synthesized published data on seagrass ammonium uptake rates to place our results in a wider context. 2. Methods [1]¿p#1 newcommands Plant collection and maintenance The ammonium uptake and translocation experiments were conducted for four seagrass species presently found in the Caribbean region: Thalassia testudinum, Syringodium filiforme, Halodule wrightii and Halophila stipulacea (Fig. 1) . The plants used in this experiment all originated from Lac Bay, a shallow lagoon (maximum 5 m deep) with calcium carbonate sediment on the Caribbean island of Bonaire. This bay has a low to moderate eutrophication status, which has been increasing over time (Govers et al. , 2014; Ouwersloot, 2022; Smulders et al. , 2022). Ammonium is the dominant source of inorganic N in both porewater and surfacewater in this system (Table S1), similar as found in similar tropical carbonate systems (McGlathery et al. , 2001; Fourqurean et al. , 2015; den Haan et al. , 2016). After collection in the field, the plants were grown in a seagrass nursery. In the nursery, seagrasses were grown on coral sand in mixed-species aquaria with artificial seawater (made by mixing Aqua Medic Reef Salt - with trace elements, without NP - and demineralized water). The nursery was situated in a climate-regulated room (25 °C), at a light intensity of 250-450 µmol m -2 s -1 (12:12 h light: dark cycle, BeamsWork HI-Lumen 60 aquarium) and with continuous aeration and water flow. Once per week, a quarter of the seawater was renewed and salinity (32 to 35 psu) and pH (8.0-8.2) were monitored twice per week. About five grams of osmocote (Osmocote, NPK 14:14:14) was added periodically to the sediment to maintain suitable nutrient conditions. This was kept at oligotrophic levels to ensure plant productivity while preventing algal overgrowth. The plants were maintained for a minimum of 1 month under standardized nursery conditions to ensure recovery from transplantation, allowing for controlled comparison of ammonium uptake rates among species. Figure 1. Study species (a) Native climax species Thalassia testudinum, (b) native opportunistic species Syringodium filiforme, (c) native pioneer species Halodule wrightii, and (d) invasive pioneer species Halophila stipulacea. Shoot and root sizes vary depending on local environmental conditions; the dimensions presented in the drawings represent average plant sizes observed in Lac Bay, Bonaire. Images taken from https://ian.umces.edu/media-library. Experimental setup A novel incubation chamber was designed using 250 ml BOROSIL glass bottles to estimate the ammonium uptake rates of above- and belowground tissues separately (Fig. 2). The bottle caps were modified by drilling holes of 14 mm diameter in the center. Two caps were then stuck together using an adhesive and metal wire. The selected plants were of similar size and morphology per species (see Figure S1, Table S2), and consisted of one shoot. The individual plants were inserted in rubber corks with pre-drilled holes and sealed with a non-toxic aquarium/terrarium adhesive (JBL Haru non-toxic universal adhesive) to prevent leakage between the two bottles. Next, the corks were inserted in the modified caps before the bottles were attached to the caps on either side to create separate above- and belowground incubation chambers. Prior to the experiments, each bottle was filled separately with artificial seawater and tested for leakage for 1-2 min with the caps and plants attached to them. The belowground chambers were wrapped in aluminium foil to prevent light from entering and placed horizontally beneath the LEDs to ensure the seals remained tight throughout the incubation. Figure 2. The experimental set-up with T. testudinum shoots as an example. (a) a single shoot was fitted through a rubber cork covered with waterproof aquarium glue. The cork was inserted in modified bottle caps, (b) attached to glass bottles and (c) placed horizontally underneath the LEDs. The root compartment was covered in aluminium foil before the start of the experiment. [1]¿p#1 newcommands Ammonium uptake experiment The ammonium uptake rates by above- and belowground tissues of all four seagrass species was determined using 15 N-labelled ammonium (Aldrich ammonium- 15 N chloride, atom % 15 N ≥ 98) at five different concentrations: 0, 5, 15, 50, and 100 μM ( n = 3). These concentrations were selected based on ammonium uptake kinetics previously reported for our study species where concentrations up to 100 μM led to ammonium saturation without causing toxicity (Lee & Dunton, 1999; Touchette & Burkholder, 2000; Alexandre et al. , 2014). The amount of 15 NH 4 Cl (mg) dissolved in artificial seawater for each incubation was used to calculate the initial substrate concentrations (S i ) ( supplementary Table S3). The aboveground chamber with leaves (leaf uptake) or the belowground chamber (root uptake) was filled with artificial seawater with 15 N-labelled ammonium, while the opposite chamber was filled with artificial seawater without added nutrients. The incubations were conducted in an artificial seawater medium at 25 °C, with a salinity of 32 g/l and a pH of 8.0-8.2. Light intensity was maintained at 200 μmol/m 2 /s throughout the experiment using LED fixtures of length 60-80 cm (BeamsWork HI-Lumen 60 aquarium). The LED fixtures were positioned so that all incubation chambers were under the light source throughout the experiment. Based on the results of a pilot experiment using T. testudinum (see supplementary Figure S2) an incubation period of 2 h was chosen to allow measurable incorporation of ammonium into plant tissues without causing substantial depletion of ammonium from the surrounding medium. At the end of each incubation, the aboveground (leaves) and belowground parts (roots and rhizomes) were separated from the cork, cleaned in artificial seawater, and oven dried (≥ 48 h at 60 o C). For T. testudinum plants, the belowground tissues were split into roots and rhizomes. However, for the analysis of belowground uptake rates of T. testudinum only root biomass was taken into consideration as rhizomes significantly increase belowground biomass but contribute minimally to nutrient absorption. (Stapel et al. , 1996). Furthermore, for the aboveground tissues of T. testudinum , leaf sheets of old leaves were discarded, and only green leaves were dried. The dried plant parts were weighed and ground into a homogeneous powder using a mortar and pestle before 15 N isotope analysis using an Isotope Ratio Mass Spectrometer (Delta XP Advantage, Thermo, Germany). Seagrass plants not exposed to 15 N-ammonium (0 μM exposure samples) were used to estimate background 15 N levels in the plant tissues. For the H. wrightii leaf uptake experiment, one replicate sample did not yield sufficient biomass material to perform isotope analysis, resulting in two control replicates for this species. Uptake and translocation calculations For all four species, we calculated the uptake of ammonium based on the enrichment of 15 N in each plant part by subtracting background 15 N values measured in control samples from the 15 N measured in plant samples after each 2 h incubation (Viana et al. , 2019) (Eq. 1): \({15N\ enrichment}_{(\mu mol)}=\frac{\left(F_{15N,sample}-\ F_{15N,background}\right)\ \times\ F_{TN,sample}\text{\ ×\ }\text{DW}_{g,sample}}{molar\ mass\ of\ 15N}\) (Eq. 1) where, 15N enrichment (µmol) is the 15 N enrichtment per plant part (leaf, root, rhizome), F 15N,sample is the atom fraction of 15 N measured after the experiment (AT% 15N ), F 15N,background is the atom fraction of 15 N measured in 0 μM exposure samples (AT% 15N ), F TN,sample is the fraction of nitrogen measured in each plant part, DW g,sample is the dry weight of the sample (g). The molar mass of 15 N is 15 x 10 -6 g/μmol. Next, we estimated the total amount of 15 N taken up by the whole plant (15N μmol,plant , μmols) as a summation of 15 N enrichment in all plant parts per replicate. [1]¿p#1 newcommands The specific uptake rate of above- or belowground tissues (V, μmol g −1 DW h −1 ), depending on the compartment that was enriched with the nutrient, was calculated by dividing the total 15 N enrichment measured in the whole plant by the incubation period (T, h) times the dry weight of the enriched plant part (DW g,enriched , g) (Eq. 3): \(V\ =\frac{{15N}_{\mu mol,plant}}{\text{DW}_{g,enriched}\times T}\) (Eq. 3) The transfer of incorporated 15 N from enriched part to the opposite plant part was assessed by expressing the enrichment of 15 N in the unexposed tissue (15N μmol,unenriched , μmol), as a percentage of the total 15 N enrichment in the whole plant (Vonk et al. , 2008) (Eq. 4): \(\%\ transfer\ =\frac{{15N}_{\mu mol,unenriched}}{{15N}_{\mu mol,plant}}\times 100\) (Eq. 4) Ammonium depletion and uptake kinetics For all experiments, the depletion of 15 N-ammonium in the water during the incubation was calculated (Eq. 5) by representing the total 15 N enrichment in the whole plant as a percentage of 15 N in 0.25 L of the incubation medium (15N μmol,medium ; μmol), based on the initial substrate concentration (Vonk et al. , 2008) (S i ): \(\%\ depletion\ =\frac{{15N}_{\mu mol,plant}}{{15N}_{\mu mol,medium}}\times 100\) (Eq. 5) Resource depletion during the uptake experiments was generally less than 2.5% (see supplementary Table S3), except for leaf uptake of T. testudinum with mean ± SD values up to 20.3% ± 10.1. Since the latter depletion rates considerably affected the exposure concentration during the incubation, we subtracted half of the depletion from the initial concentrations (S i ) to determine the exposure concentration (S c ) during these incubations (Table S3). To determine the ammonium uptake kinetic parameters V max , K m and alpha, the ammonium uptake rates with the corrected exposure concentrations were fitted to the Michaelis-Menten model, V = (V max x S c )/(S c + K m ). V is uptake rate (μmol g −1 DW h −1 ), V max is maximum uptake rate (μmol g −1 DW h −1 ), S c is the corrected exposure concentration (μM) and K m is the half-saturation constant (μmol), while alpha is the affinity constant V max /K m . Data that did not follow Michaelis Menten saturation kinetics were fitted with a linear regression model, V = a * S c , where V is uptake rate, and a is the regression slope (comparable to alpha in the Michaelis Menten model). Literature review To place the obtained ammonium uptake rates of the four studied seagrasses in a broader context, we collected studies on seagrass ammonium uptake rates from Web of Science and Google Scholar© (ISI; search: “seagrass” AND “ammonia” OR “ammonium” AND “uptake rate” OR “acquisition” OR “transfer” OR “translocation”), accessed September 1, 2025. Next, we provided an overview of available data on calculated uptake parameters based on Michaelis Menten kinetics. For synthesis, we extracted and reported data only from studies that provided uptake parameters derived from Michaelis–Menten kinetics (V max , K m ), thereby excluding studies that report uptake rates without kinetic modelling. [1]¿p#1 newcommands Statistical analysis [1]¿p#1 newcommands To test the difference in ammonium uptake rates between the species, we used two-way analyses of variance on log-transformed uptake rate data of the aboveground and belowground enrichment experiments separately, with species and ammonium concentration as the main factors that were tested separately and for an interaction effect. Significant differences were revealed with Tukey HSD post-hoc comparisons. [1]¿p#1 newcommands A similar approach was used to test for differences in ammonium transfer percentages, using two-way analyses of variance on log(x + 0.1)-transformed percentage transfer data from aboveground to belowground compartments, and square root-transformed transfer data from belowground to aboveground compartments, including species and ammonium concentration as main factors. Significant differences were revealed with Tukey HSD post-hoc comparisons. All data was analyzed using RStudio (version 2025.09.2+418). [1]¿p#1 newcommands 3. Results Ammonium uptake rates of Caribbean seagrasses The ammonium uptake rates by the leaves of two species, Halodule wrightii and Halophila stipulacea, followed Michaelis-Menten kinetics, showing a diminishing increase in uptake rate as the ammonium concentration increased (Table 1). In contrast, Thalassia testudinum and Syringodium filiforme uptake rates increased linearly with ammonium concentration, showing no saturation. The results of the two-way ANOVA confirmed the non-parallel trends between species, with a significant interaction effect between species and ammonium concentration (df = 9, F = 2.378, p < 0.05). Ammonium concentration strongly affected leaf uptake rates (df = 3, F = 104.9, p < 0.001). When all species were grouped, leaf uptake rates increased significantly between each combination of ammonium concentrations (Tukey post-hoc pairwise comparisons; p < 0.01). However, there was no significant effect of seagrass species on leaf uptake rates and therefore uptake rates of H. stipulacea were not significantly higher than those of the native species. Table 1. The uptake parameters based on Michaelis Menten kinetics as obtained from our experiment (maximum uptake rate (V max , μmol g −1 DW h −1 ), half saturation constant (K m, µM), affinity coefficient (α, V max /K m ) and the regression coefficient (R 2 )). For the species and plant parts that did not follow Michaelis-Menten saturation kinetics, a linear regression model was fitted and the formula is presented together with the regression coefficient. Leaf Thalassia testudinum V = 0.1 * S 0.88 Syringodium filiforme V = 0.1 * S 0.91 Halodule wrightii 8.0 32.4 0.2 0.50 Halophila. stipulacea 33.6 295 0.1 0.88 Root Thalassia.testudinum 1.8 104 0.02 0.79 Syringodium filiforme 0.7 40.6 0.02 0.87 Halodule wrightii 1.4 19.7 0.07 0.51 Halophila stipulacea V = 0.01 * S 0.89 The ammonium uptake rates by the belowground parts followed Michaelis-Menten kinetics for all species except for H. stipulacea, which exhibited a linear, non-saturating response. Belowground uptake rates differed significantly between species and among ammonium concentrations (Two-way ANOVA; df = 3, F = 17.05, p < 0.001; and df = 3, F = 80.46, p < 0.001; respectively). Additionally, a significant interaction effect was found between species and ammonium concentration (df = 9, F = 2.977, p < 0.05), indicating that the differences in uptake rates among species were not consistent across all ammonium concentrations, likely due to H. stipulacea’ s linear response. Overall, H. wrightii had significantly higher belowground uptake rates compared to H. stipulacea (Tukey post-hoc pairwise comparisons, p < 0.001), S. filiforme ( p < 0.001), and T. testudinum ( p < 0.01). Additionally, T. testudinum had higher uptake rates than H. stipulacea ( p < 0.05). When considering the effect of concentration, belowground uptake rates differed significantly between each concentration ( p < 0.001) except between 50 µM and 100 µM ( p = 0.056). To further investigate the interaction effect, pairwise comparisons of belowground uptake rates at each concentration showed that at 5 µM, both H. wrightii and T. testudinum were significantly higher than H. stipulacea ( p < 0.001). At 15 µM, H. wrightii was significantly higher than H. stipulacea ( p < 0.05), while at 50 µM, H. wrightii was significantly higher than S. filiforme ( p < 0.05). At 100 µM, there were no significant differences between the species. Figure 3 . Mean ± SE values ( n = 3) of the uptake rates (µM NH 4 g -1 DW h -1 ) of the leaves (above) and the roots (below) of the four Caribbean seagrasses Thalassia testudinum (purple) , Syringodium filiforme (aquamarine) , Halophila stipulacea (red) and Halodule wrightii (green), measured using 15 N-labeled NH 4 + after 2 h incubations. The best fit models are plotted, either Michaelis-Menten (curves) or linear regressions. [1]¿p#1 newcommands Ammonium transfer in Caribbean seagrasses The percentage transfer of ammonium from leaves to roots differed significantly between the species (df = 3, F = 9.381, p < 0.001); H. wrightii leaves transferred a significantly higher percentage of ammonium to the roots compared H. stipulacea ( p = 0.01) and S. filiforme ( p < 0.001). T. testudinum also showed a significantly higher leaf-to-root transfer compared to S. filiforme ( p < 0.01). The percentage transfer of ammonium from roots to leaves differed significantly between species (df = 3, F = 30.77, p < 0.001), and between concentrations (df = 3, F = 4.639, p < 0.001), with a significant interaction effect between species and ammonium concentration (df = 9, F = 13.09, p < 0.001). Tukey post-hoc pairwise comparisons revealed that H. stipulacea, S. filiforme, and T. testudinum all had significantly higher transfer from roots to leaves compared to H. wrightii ( p < 0.05). Additionally, both T. testudinum and S. filiforme had significantly higher root-to-leaf transfer than H. stipulacea ( p < 0.001). For all species, the percentage transfer was significantly lower at 50 µM ammonium compared to 5 µM ammonium. Pairwise comparisons at each concentration showed that again, H. wrightii had significantly lower transfer at 5 µM compared to S. filiforme and T. testudinum. At 15 µM, S. filiforme had higher transfer compared to H. wrightii. At 50 µM, T. testudinum had significantly higher transfer than H. stipulacea, and lastly at 100 µM, H. stipulacea had significantly higher transfer than H. wrightii. Pairwise comparisons per species showed that H. stipulacea percentage transfer was significantly higher at 100 µM than at 50 µM and 5 µM, T. testudinum was significantly higher at 100 µM, 50 µM and 15 µM compared to 5 µM, while H. wrightii and S. filiforme showed no significant differences in relative transfer of ammonium between concentrations. Figure 4. Transfer (%) of 15 N taken up by native Thalassia testudinum, Syringodium filiforme and Halodule wrightii and invasive Halophila stipulacea comparing transfer from (a) leaves to roots and (b) roots to leaves. Overview of available data on ammonium uptake kinetics of seagrasses From the literature, we obtained 50 studies investigating ammonium uptake rates in seagrasses (supplementary Table S4). These studies covered 19 species, with temperate species forming the majority (57%) and tropical species covering the remaining part (43%). Most studies reported values for single species, while 16% included two or more species. For H. stipulacea , S. filiforme, and H. wrightii, there was only one previous study, the one on H. stipulacea collected from its Mediterranean invaded habitat. The methods used to obtain uptake rates could be categorized in three groups: 61% used labeled 15 N methods, 22% calculated depletion of ammonium from the incubated medium, and 17% used flume methods. The studies that calculated ammonium transfer all used labelled 15 N methods. Out of 50, 13 studies calculated uptake parameters based on Michaelis Menten kinetics (Table 2), and five calculated the percentage of ammonium transfer between plantparts (Table 3). Overall, the reported maximum leaf uptake rates (V max ) showed over three orders of magnitudes differences and varied from 0.15 ( Cymodocea nodosa ) to 204 ( Phyllospadix torrey ) μmol NH 4 + g −1 DW h −1 . The half-saturation constants (K m ) varied from 5.1 ( T. testudinum ) to 241.3 ( H. stipulacea ) µM ammonium. Similarly. the variation in reported affinity constants of leaves ( α) was over three orders of magnitude and varied from 0.002 ( C. nodosa ) to 2.8 ( T. testudinum ). For the belowground or root uptake rates, the maximum uptake rates (V max ) varied more than three orders of magnitude from 0.04 ( C. nodosa ) to 211 ( Zostera marina ) μmol NH 4 + g −1 DW h −1 . For the half-saturation constant (K m ) over two orders of magnitude differences were reported, varying from 4.8 ( A. antarctica ) to 765.5 ( T. testudinum ) µM ammonium. The variation in reported affinity constants of the belowground part ( α) was again more than three orders of magnitude and varied from 0.0004 ( C. nodosa ) to 2.0 ( Z. marina ). Comparing the different methods, the average (± SE) affinity constant (α) used with the method of depletion N ± SE in substrate was 1.0 ± 0.4 for the leaves and 0.8 ± 0.6 for the roots compared to 0.3 ± 0.1 for leaves and 0.08 ± 0.03 for roots as found by the 15 N labelling experiments. There was also a high variation in studied concentration ranges, with maximum concentrations varying from 7 – 300 µM. Temperate species had an average α of 0.8 ± 0.3 for the leaves and 0.6 ± 0.5 for the roots, while tropical species had slightly lower α values: 0.6 ± 0.4 for the leaves and 0.1 ± 0.05 for the roots, respectively. The transfer data indicates in general higher root-to-leaf transfer (ranging from 0 to 55%) than leaf-to-root (ranging from 0 to 22%) with high variation between species and ammonium exposure concentrations (Table 3). Table 2. An overview of uptake parameters based on Michaelis Menten kinetics (maximum uptake rate (V max , μmol NH 4 + g −1 DW h −1 ), half saturation constant (K m, µM), affinity coefficient (α, V max /K m )), ammonium concentrations (µM) and incubation time (h) used as reported in the literature using varying methods, compared to those found in this study. Results that did not follow Michaelis-Menten saturation kinetics but instead were fitted with a linear regression model are indicated with an ‘L’. We present separate lines per plant part enriched with ammonium, per study, and per species. A range is provided when multiple values were reported for the same species and method. Species V max K m α Concentration Time Method Source Leaf Temperate Amphibolis antarctica L L n.a. [0.35 – 7.14] 2 Depletion N Paling et al., 1994 Amphibolis antarctica 6.0 – 43.1 9.5 – 74 0.6 – 0.8 [3.5 – 85] 0 – 4 Depletion N Pedersen et al., 1997 Cymodocea nodosa 14.9 44.4 0.3 [5 – 100] 1 15 N label Alexandre et al., 2020a Cymodocea nodosa 0.15 93.0 0.002 [0.5 – 200] 1 15 N label Alexandre et al., 2020b Phyllospadix iwatensis 2.2 – 35.5 12.7 – 134 0.12 – 0.28 [2 – 40] 2 – 4 Depletion N Hasegawa et al., 2005 Phyllospadix torrey 95.6 – 204 9.3 – 33.9 - [1 – 32] 2 – 3 Depletion N Terrados et al., 1997 Zostera marina 20.5 9.2 2.2 [3 - 45] 0.8 – 2.5 Depletion N Thursby et al., 1982 Zostera noltii 28.3 28.7 1.0 [5 – 100] 1 15 N label Alexandre et al., 2011 Zostera noltii L L n.a. [0 – 100] 2 Depletion N Villazán et al., 2013 Tropical Halodule wrightii 8.0 32.4 0.2 [5 – 100] 2 15 N label This study Halophila stipulacea 9.8 58.0 0.2 [5 – 100] 12 15 N label Alexandre et al., 2014 Halophila stipulacea 33.1 295 0.1 [5 – 100] 2 15 N label This study Syringodium filiforme 0.1*S L n.a. [5 – 100] 2 15 N label This study Thalassia hemprichii 32 – 37 21 – 60 0.1 – 0.2 [4 – 150] 1 Depletion N Stapel et al., 1996 Thalassia hemprichii 37.4 – 37.9 67.9 – 76.9 0.49 – 0.55 [1 – 180] 2 Depletion N Zhang et. al. 2011 Thalassia testudinum 8.5 - 16.4 5.1 – 19.4 0.6 – 2.8 [3 - 200] 1 – 2 Depletion N Lee et al., 1999 Thalassia testudinum 0.1*S L n.a. [5 – 100] 2 15 N label This study Root Temperate Amphibolis antarctica 1.1 4.8 0.2 [3.5 – 85] 2 15 N label Pedersen et al., 1997 Cymodocea nodosa 0.01*S L n.a. [5 – 100] - 15 N label Alexandre et al., 2020a Cymodocea nodosa 0.04 92.7 0.0004 [0.5 – 200] 1 15 N label Alexandre et al., 2020b Phyllospadix iwatensis 0.5 61.3 0.01 [2 – 40] 2 – 4 Depletion N Hasegawa et al 2005 Zostera marina 211 104 2.0 [3 - 150] 0.8 – 2.5 Depletion N Thursby et al., 1982 Zostera noltii 3 52.5 0.06 [5 – 100] 1 15 N label Alexandre et al., 2011 Tropical Halodule wrightii 1.4 19.7 0.07 [5 – 100] 2 15 N label This study Halophila stipulacea 6.1 30.9 0.2 [5 – 100] 12 15 N label Alexandre et al., 2014 Halophila stipulacea 0.01*S L n.a. [5 – 100] 2 15 N label This study Syringodium filiforme 0.7 40.6 0.02 [5 – 100] 2 15 N label This study Thalassia hemprichii 25.9 – 31.3 36.9 – 43.9 0.7 [1 – 180] 2 Depletion N Zhang et. al. 2011 Thalassia testudinum 7.9 – 73.3 34.4 – 766 0.03 – 0.3 [3 - 200] 1 – 2 Depletion N Lee et al., 1999 Thalassia testudinum 1.8 103.8 0.02 [5 – 100] 2 15 N label This study Table 3. An overview of nitrogen transfer data as reported in literature and found in this study, expressed as percentage of ammonium-N uptake, calculated by dividing the µ mol 15 N in the unenriched plant part divided by the total µ mol 15 N enrichment in the plant. Transfer was calculated after incubation durations ranging from 1 – 12 h after exposure to varying ammonium concentrations ( µ M). Species Transfer Time Concentration Source Leaf-to-root Temperate Cymodocea nodosa 13 – 22 1 [5 – 100] Alexandre et al., 2020 Zostera nigricaulis 3 2 13.7 Nayar et al., 2018 Zostera nigricaulis 0 2 13.7 Nayar et al., 2018 Zostera nigricaulis 2 2 13.7 Nayar et al., 2018 Zostera noltii < 1 1 [5 – 100] Alexandre et al., 2011 Tropical Oceana serrulata 5.17 1 20 Viana et al., 2019 Halodule wrightii 2.4 – 11.5 2 [5 – 100] This study Halophila stipulacea 0.0 – 2.1 2 [5 – 100] This study Halophila stipulacea < 2.5 12 [5 – 100] Alexandre et al., 2014 Syringodium filiforme 0 – 0.3 2 [5 – 100] This study Thalassia hemprichii 2.9 1 20 Viana et al., 2019 Thalassia testudinum 0.5 – 9.4 2 [5 – 100] This study Root-to-leaf Temperate Cymodocea nodosa 6– 13 1 [5– 100] Alexandre et al., 2020 Zostera nigricaulis 18 2 13.7 Nayar et al., 2018 Zostera nigricaulis 32 2 13.7 Nayar et al., 2018 Zostera nigricaulis 23 2 13.7 Nayar et al., 2018 Zostera noltii < 1 1 [5 – 100] Alexandre et al., 2011 Tropical Oceana serrulata 9.7 1 20 Viana et al., 2019 Halodule wrightii 0 – 1.7 2 [5 – 100] This study Halophila stipulacea < 2.5 12 [5 – 100] Alexandre et al., 2014 Halophila stipulacea 0.5 – 17.8 2 [5 – 100] This study Syringodium filiforme 4.0 – 21.4 2 [5 – 100] This study Thalassia hemprichii 10.3 1 20 Viana et al., 2019 Thalassia testudinum 3.7 – 55.3 2 [5 – 100] This study 4. Discussion Nutrient uptake plasticity underpins invasion potential Nutrient uptake strategies are key determinants of plant competitive ability and invasion success (Blumenthal, 2006; Funk & Vitousek, 2007; Littschwager et al. , 2010). In seagrasses, ammonium is the primary source of inorganic nitrogen supporting high primary productivity across most tropical seagrass meadows (Burkholder et al. , 2007) . Using isotopic enrichment incubations, we compared ammonium uptake kinetics among four Caribbean seagrasses, including the invasive Halophila stipulacea . We found that at current ammonium concentrations, invasive seagrass does not hold a competitive advantage. However, substantial interspecific variation in leaf and root uptake affinity and internal nitrogen transfer revealed distinct nutrient-use strategies that may mediate coexistence and invasion dynamics under changing nutrient regimes. Native Caribbean seagrasses generally maintain higher root uptake rates (notably Halodule wrightii and Thalassia testudinum ) and more efficient bidirectional transfer between leaves and roots, whereas the invasive H. stipulacea showed lower root uptake rates but relatively efficient root-to-leaf transfer under high ammonium supply . This pattern indicates greater plasticity in nutrient allocation rather than superior overall uptake capacity. Such physiological flexibility allows H. stipulacea to shift resource acquisition toward the plantpart most exposed to available nitrogen, while maintaining high rates of biomass turnover, a trait commonly associated with successful plant invasions (Funk, 2013). Although H. stipulacea did not outperform native species under oligotrophic conditions, its high maximum leaf uptake rate, and elevated half-saturation constant suggest a capacity to exploit transient nutrient pulses more effectively. While ammonium concentrations in the water column are typically low, leaf uptake likely contributes substantially to the overall nitrogen budget of the plant (Marbà et al. , 2002; Alexandre et al. , 2011b) , and can therefore be crucial for invasion success. For instance, during episodic nutrient surges, caused by land runoff or sediment disturbances mobilizing porewater ammonium into the water column, the contribution of leaf ammonium uptake may even exceed root uptake (Alexandre & Santos, 2020b) . The global synthesis revealed that the leaf uptake parameters measured here for H. stipulacea rank among the highest reported for any seagrass species, supporting the idea that rapid nutrient assimilation during enrichment events could underpin competitive displacement of native species in eutrophic coastal habitats, leading to reverse succession and dominance of invasive seagrass (Figure 5). The plasticity in uptake kinetics mirrors patterns seen in other marine invaders such as Caulerpa spp. (Gennaro & Piazzi, 2011; Gennaro et al. , 2015; Alexandre & Santos, 2020b) , where physiological responsiveness drives invasion success. Figure 5. Conceptual diagram of our results. Succession in oligotrophic tropical environments typically follows the trajectory of seagrass pioneer species to climax species over time. This order of succession may be reversed due to the variation in nutrient uptake and allocation strategy and plasticity, under influence of (temporarily) elevated ammonium concentrations in the water and accumulation in the sediment. Where native climax species and pioneer species profit from low to moderate ammonium concenctrations by efficient root and leaf uptake and transfer, the exotic pioneer Halophila stipulacea invests in rapid leaf production and root-to-leaf transfer under elevated ammonium concentrations. Allocation trade-offs define contrasting nutrient-use strategies Among native species, the pioneer H. wrightii exhibited high root and leaf affinity (α, V max /K m ), which, together with consistently higher root uptake rates across ammonium concentrations compared to the other species indicates a broad functional niche that may stabilize its persistence under moderate enrichment, corresponding to H. wrightii dominance in high-nutrient environments (Fourqurean et al. , 1992) . The climax species T. testudinum, adapted to stable oligotrophic sediments, maintained superior root uptake relative to the invasive pioneer species H. stipulacea, particularly at low concentrations (5 µM), supporting its competitive advantage under nutrient-poor conditions. Similarly, Syringodium filiforme and T. testudinum exhibited high internal nutrient transfer efficiency at ≤50 µM compared to the native and invasive pioneer species, potentially enabling flexible nitrogen redistribution during short-term fluctuations in oligotrophic to moderately enriched habitats. Halophila stipulacea , by contrast, demonstrated a marked allocation bias under nutrient enrichment: efficient root-to-leaf transfer at high ammonium concentrations (18%, compared to ≤1% in H. wrightii ). This pattern suggests that the invader invests preferentially in rapid leaf production when nutrients are abundant, consistent with its opportunistic life history and high turnover rates (O’Brien et al. , 2018), and consistent with previous field assessments of H. stipulacea translocation strategy in its native region (Marbà et al. , 2002). Allocation trade-offs such as sustained root efficiency in native climax species and dynamic above-ground allocation in the invader, may determine the outcome of competitive interactions as environmental nutrient levels rise. Importantly, the observation that several species did not reach uptake saturation at 100 µM ammonium indicates that the presented uptake capacities may be underestimated , particularly under high eutrophic conditions where porewater ammonium concentrations can exceed 150 µM (Fourqurean et al. , 1992; Lee & Dunton, 2000) . Expanding future assays to higher concentrations will help define thresholds beyond which physiological toxicity or diminishing returns constrain uptake efficiency. Environmental thresholds govern context-dependent competitiveness The ecological implications of these mechanistic differences depend strongly on environmental context. Invasive macrophytes can either outcompete native species or opportunistically colonize vacant niches. Evidence for direct competition between native seagrass and invasive H. stipulacea remains limited (Winters et al. , 2020) . However, H. stipulacea has been shown to reduce native shoot production in some cases (Chiquillo et al. , 2023) . Under the low to moderate ammonium concentrations typical of Caribbean waters (0 – 50 µM) (McGlathery et al. , 2001; Fourqurean et al. , 2015) , native species maintain higher uptake and transfer efficiency than invasive H. stipulacea and therefore other physical disturbances such as hurricanes or grazing pressure may primarily drive declines of climax species and open up niches for invasives seagrass (Christianen et al. , 2019; Hernández-Delgado et al. , 2020) . Indeed our measured average field ammonium concentrations, 59 µM and 57 µM for sediment porewater and surface water respectively, at our sampling site of Bonaire, would imply a physiological advantage for the native seagrasses. However, nutrient levels in this region have roughly doubled over the past decade (porewater total N ~25 µM reported by Govers et al. , 2014) and are expected to continue rising nearshore Caribbean waters due to terrestrial overgrazing, erosion-driven runoff, inadequate wastewater treatment, and Sargassum decomposition (van Tussenbroek et al. , 2017; Rivas et al. , 2020) . While light limitation and sedimentation are likely the dominant impacts of these anthropogenic stressors on seagrass ecosystems, the enhanced mineralization of organic matter, including the reduction of nitrate, within oxygen-poor sediments trapped within meadows can increase sediment ammonium levels, thereby influencing competitive interactions among species with differing uptake efficiencies (Touchette & Burkholder, 2000; de Boer, 2007; Serrano et al. , 2016) . Furthermore, as fine sediments have been found to accumulate in H. stipulacea meadows (James et al. , 2020) , this species may further facilitate its own microhabitat and therefore increase their invasion potential. Our findings suggest that once ammonium concentrations exceed 100 µM, H. stipulacea may cross a physiological threshold that enhances competitiveness through rapid nutrient assimilation and preferential allocation to above-ground tissues. This context-dependent advantage highlights the importance of trait–environment interactions in invasion ecology: physiological traits confer success only under environmental regimes that match their performance optima (Muthukrishnan et al. , 2020) . In this case, H. stipulacea ’s opportunistic uptake strategy positions it to benefit disproportionately from anthropogenic nutrient enrichment, paralleling the behavior of other invaders in both marine and terrestrial ecosystems (Littschwager et al. , 2010; Gennaro et al. , 2015; Sardans et al. , 2017) . Linking physiological divergence to invasion success Comparisons between invaded regions reveal further evidence of plasticity and potential local adaptation. Maximum leaf ammonium uptake rates of Caribbean H. stipulacea measured in our study were more than threefold higher than those reported for Mediterranean populations, and root uptake did not saturate at 100 µM, in contrast to the Mediterranean plants (Alexandre et al. , 2014) . Similarly, measured internal transfer rates (root-to-leaf) in the Caribbean (up to 18%), far exceeded those reported in the Mediterranean (2.5%). These differences suggest that the physiology of H. stipulacea varies between invaded regions, potentially reflecting genetic differentiation or phenotypic acclimation to local nutrient regimes. The species spread rate further supports this view, covering ~2400 km across the Caribbean within 23 years (Ruiz & Ballantine, 2004; Campbell et al. , 2025) , compared to ~2800 km over 150 years in the Mediterranean (pers. comm. F. Tomas-Nash). Such divergence aligns with earlier observations of enhanced growth and photosynthetic traits in Caribbean populations (Winters et al. , 2023) . However, our literature synthesis also revealed pronounced intraspecific variability in uptake parameters, even within single regions (e.g. Cymodocea nodosa in Mediterranean lagoons; (Alexandre & Santos, 2020a,b ). Replicated physiological comparisons of H. stipulacea populations across native and invaded ranges are therefore needed to link physiological traits with invasion success. [1]¿p#1 newcommands Methodological advances and global synthesis A key contribution of this study is methodological: the application of a low-cost split-chamber incubation system, separated by a rubber cork, that enabled independent quantification of above- and belowground nutrient uptake of four morphologically different seagrasses using 15 N tracers. This approach reduces uncertainties associated with nutrient depletion techniques, which may overestimate uptake rates, potentially due to unaccounted background fluxes or losses via sorption (Romero et al. , 2006). The chambers provide a standardized, replicable method suitable for a broad range of seagrass species, and using the same method to study different seagrass species will facilitate cross-species and cross-study comparison. Our literature synthesis reveals that ammonium uptake kinetic parameters and transfer rates have been quantified for only 12 out of ~60 seagrass species, leaving significant gaps (particularly from the species-rich Indo-Pacific region) in understanding nitrogen acquisition within this key functional group and identifying most reliable methods to obtain kinetic parameters. Expanding such trait-based datasets is essential for incorporating seagrasses into global models of plant nutrient economics and invasion dynamics. Future work should control for plant physiological history, as pre-exposure to stressors such as heatwaves or ocean acidification can alter nutrient uptake and assimilation (Pazzaglia et al. , 2022; Berlinghof et al. , 2024; Bass et al. , 2025) . Standardizing experimental conditions will improve cross-system and interspecific comparability and enhance the predictive power of seagrass nutrient models. Similar to the leaf-to-root transfer rates measured in our experiment, the variation in transfer rates as obtained from literature show high variation and limited understanding of transfer rates across species, which should be looked into in future studies. [1]¿p#1 newcommands Conclusions and broader implications Collectively, our findings demonstrate that native Caribbean seagrasses are well adapted to oligotrophic conditions through high ammonium affinity and balanced internal nutrient redistribution. In contrast, invasive H. stipulacea relies on root-to-leaf allocation plasticity and rapid leaf uptake at high ammonium concentrations to exploit nutrient pulses, potentially reversing the order of succession in habitats prone to eutrophication. These contrasting strategies illustrate a fundamental trade-off between efficiency and flexibility in plant nutrient acquisition—a general principle that governs coexistence and invasion potential across ecosystems (Matzek, 2011; Muthukrishnan et al. , 2020). As nutrient loading in Caribbean coastal waters continues to rise , such environmental shifts are likely to cross thresholds favoring opportunistic invaders like H. stipulacea . Linking physiological uptake traits to nutrient regimes thus provides a mechanistic basis for predicing changes in community composition and productivity. By identifying the thresholds at which nutrient enrichment alters competitive hierarchies, management interventions can be prioritized to maintain native seagrass dominance and ecosystem function under accelerating coastal change. References Alexandre A, Georgiou D, Santos R . 2014 . Inorganic nitrogen acquisition by the tropical seagrass Halophila stipulacea . Marine Ecology 35 : 387–394. Alexandre A, Santos R . 2020a . Nutrition of the seagrass Cymodocea nodosa : Pulses of ammonium but not of phosphate are crucial to sustain the species growth. Marine Environmental Research 158 : 104954. Alexandre A, Santos R . 2020b . Competition for nitrogen between the seaweed Caulerpa prolifera and the seagrass Cymodocea nodosa . Marine Ecology Progress Series 648 : 125–134. Alexandre A, Silva J, Bouma TJ, Santos R . 2011a . Inorganic nitrogen uptake kinetics and whole-plant nitrogen budget in the seagrass Zostera noltii . Journal of Experimental Marine Biology and Ecology 401 : 7–12. Alexandre A, Silva J, Bouma TJ, Santos R . 2011b . Inorganic nitrogen uptake kinetics and whole-plant nitrogen budget in the seagrass Zostera noltii . Journal of Experimental Marine Biology and Ecology 401 : 7–12. Bass A V., Wang Z, Chung NM, So MWK, Falkenberg LJ, Thibodeau B . 2025 . Altered nutrient cycling functionality in seagrass meadows under a simulated future marine heatwave event. New Phytologist 247 : 2616–2629. Berlinghof J, Montilla LM, Peiffer F, Quero GM, Marzocchi U, Meador TB, Margiotta F, Abagnale M, Wild C, Cardini U . 2024 . Accelerated nitrogen cycling on Mediterranean seagrass leaves at volcanic CO2 vents. Communications Biology 7 : 341. Blumenthal DM . 2006 . Interactions between resource availability and enemy release in plant invasion. Ecology Letters 9 : 887–895. de Boer WF . 2007 . Seagrass–sediment interactions, positive feedbacks and critical thresholds for occurrence: a review. Hydrobiologia 591 : 5–24. Burkholder JM, Tomasko DA, Touchette BW . 2007 . Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350 : 46–72. Campbell JE, Allen A-C, Sattelberger DC, White MD, Fourqurean JW . 2025 . First record of the seagrass Halophila stipulacea (Forsskal) Ascherson in the waters of the continental United States (Key Biscayne, Florida). Aquatic Botany 196 : 103820. Chiquillo KL, Barber PH, Vasquez MI, Cruz‐Rivera E, Willette DA, Winters G, Fong P . 2023 . An invasive seagrass drives its own success in two invaded seas by both negatively affecting native seagrasses and benefiting from those costs. Oikos 2023 . 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 (K Van Alstyne, Ed.). Journal of Ecology 107 : 45–57. Dunic JC, Brown CJ, Connolly RM, Turschwell MP, Côté IM . 2021 . Long-term declines and recovery of meadow area across the world’s seagrass bioregions. Global Change Biology 27 : 4096–4109. Fourqurean JW, Manuel SA, Coates KA, Kenworthy WJ, Boyer JN . 2015 . Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda. Biogeosciences 12 : 6235–6249. Fourqurean JW, Powell GVN, Kenworthy WJ, Zieman JC . 1995 . The Effects of Long-Term Manipulation of Nutrient Supply on Competition between the Seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. Oikos 72 : 349. Fourqurean JW, Zieman JC, Powell GVN . 1992 . Relationships between porewater nutrients and seagrasses in a subtropical carbonate environment. Marine Biology 114 : 57–65. Funk JL . 2013 . The physiology of invasive plants in low-resource environments. Conservation Physiology 1 : cot026–cot026. Funk JL, Vitousek PM . 2007 . Resource-use efficiency and plant invasion in low-resource systems. Nature 446 : 1079–1081. Gennaro P, Piazzi L . 2011 . Synergism between two anthropic impacts: Caulerpa racemosa var. cylindracea invasion and seawater nutrient enrichment. Marine Ecology Progress Series 427 : 59–70. Gennaro P, Piazzi L, Persia E, Porrello S . 2015 . Nutrient exploitation and competition strategies of the invasive seaweed Caulerpa cylindracea . European Journal of Phycology 50 : 384–394. Govers LL, Lamers LPM, Bouma TJ, de Brouwer JHF, van Katwijk MM . 2014 . Eutrophication threatens Caribbean seagrasses – An example from Curaçao and Bonaire. Marine Pollution Bulletin 89 : 481–486. den Haan J, Huisman J, Brocke HJ, Goehlich H, Latijnhouwers KRW, van Heeringen S, Honcoop SAS, Bleyenberg TE, Schouten S, Cerli C, et al. 2016 . Nitrogen and phosphorus uptake rates of different species from a coral reef community after a nutrient pulse. Scientific Reports 6 : 28821. Hernández-Delgado EA, Toledo-Hernández C, Ruíz-Díaz CP, Gómez-Andújar N, Medina-Muñiz JL, Canals-Silander MF, Suleimán-Ramos SE . 2020 . Hurricane Impacts and the Resilience of the Invasive Sea Vine, Halophila stipulacea : a Case Study from Puerto Rico. Estuaries and Coasts 43 : 1263–1283. James RK, Christianen MJA, Katwijk MM, Smit JC, Bakker ES, Herman PMJ, Bouma TJ . 2020 . Seagrass coastal protection services reduced by invasive species expansion and megaherbivore grazing (AR Hughes, Ed.). Journal of Ecology 108 : 2025–2037. Krause JR, Cameron C, Arias-Ortiz A, Cifuentes-Jara M, Crooks S, Dahl M, Friess DA, Kennedy H, Lim KE, Lovelock CE, et al. 2025 . Global seagrass carbon stock variability and emissions from seagrass loss. Nature Communications 16 : 3798. Lee K-S, Dunton KH . 1999 . Inorganic nitrogen acquisition in the seagrass Thalassia testudinum : Development of a whole-plant nitrogen budget. Limnology and Oceanography 44 : 1204–1215. Lee KS, Dunton KH . 2000 . Effects of nitrogen enrichment on biomass allocation, growth, and leaf morphology of the seagrass Thalassia testudinum . Marine Ecology Progress Series 196 : 39–48. Littschwager J, Lauerer M, Blagodatskaya E, Kuzyakov Y . 2010 . Nitrogen uptake and utilisation as a competition factor between invasive Duchesnea indica and native Fragaria vesca . Plant and Soil 331 : 105–114. Manhães AP, Pantaleão LC, Moraes LFD, Amazonas NT, Saavedra MM, Mantuano D, Sansevero JBB . 2022 . Functional trajectory for the assessment of ecological restoration success. Restoration Ecology 30 . Marbà N, Hemminga M, Mateo M, Duarte M, Mass Y, Terrados J, Gacia E . 2002 . Carbon and nitrogen translocation between seagrass ramets. Marine Ecology Progress Series 226 : 287–300. Matzek V . 2011 . Superior performance and nutrient-use efficiency of invasive plants over non-invasive congeners in a resource-limited environment. Biological Invasions 13 : 3005–3014. 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. Biological Reviews 92 : 1521–1538. McGlathery KJ, Berg P, Marino R . 2001 . Using porewater profiles to assess nutrient availability in seagrass-vegetated carbonate sediments. Biogeochemistry 56 : 239–263. McGlathery KJ, Sundbäck K, Anderson IC . 2007 . Eutrophication in shallow coastal bays and lagoons: The role of plants in the coastal filter. Marine Ecology Progress Series 348 : 1–18. Muthukrishnan R, Sullivan LL, Shaw AK, Forester JD . 2020 . Trait plasticity alters the range of possible coexistence conditions in a competition–colonisation trade‐off. Ecology Letters 23 : 791–799. Nordlund LM, Koch EW, Barbier EB, Creed JC . 2016 . Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 11 . O’Brien KR, Waycott M, Maxwell P, Kendrick GA, Udy JW, Ferguson AJP, Kilminster K, Scanes P, McKenzie LJ, McMahon K, et al. 2018 . Seagrass ecosystem trajectory depends on the relative timescales of resistance, recovery and disturbance. Marine Pollution Bulletin 134 : 166–176. Ouwersloot B . 2022 . Seagrass as bioindicator for eutrophication and pollution in the coastal bays of Bonaire, Caribbean Netherlands. Paling EI, McComb AJ . 1994 . Nitrogen and phosphorus uptake in seedlings of the seagrass Amphibolis antarctica in Western Australia. Hydrobiologia 294 : 1–4. Pazzaglia J, Santillán-Sarmiento A, Ruocco M, Dattolo E, Ambrosino L, Marín-Guirao L, Procaccini G . 2022 . Local environment modulates whole-transcriptome expression in the seagrass Posidonia oceanica under warming and nutrients excess. Environmental Pollution 303 : 119077. Pedersen MF, Paling EI, Walker DI . 1997 . Nitrogen uptake and allocation in the seagrass Amphibolis antarctica. Aquatic Botany 56 : 105–117. Rivas EJG, Pérez GR, Tundisi JG, Vammen K, Örmeci B, Forde M . 2020 . Eutrophication: A growing problem in the Americas and the Caribbean. Brazilian Journal of Biology 80 : 688–689. Romero J, Lee KS, Pérez M, Mateo MA, Alcoverro T . 2006 . Nutrient dynamics in seagrass ecosystems. In: Seagrasses: Biology, Ecology and Conservation. 227–254. Ruiz H, Ballantine DL . 2004 . Occurrence of the seagrass Halophila stipulacea in the tropical west Atlantic. Bulletin of Marine Science 75 : 131–135. Sardans J, Bartrons M, Margalef O, Gargallo‐Garriga A, Janssens IA, Ciais P, Obersteiner M, Sigurdsson BD, Chen HYH, Peñuelas J . 2017 . Plant invasion is associated with higher plant–soil nutrient concentrations in nutrient‐poor environments. Global Change Biology 23 : 1282–1291. 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. Aquatic Botany 144 : 1–8. Serrano O, Lavery P, Masque P, Inostroza K, Bongiovanni J, Duarte C . 2016 . Seagrass sediments reveal the long‐term deterioration of an estuarine ecosystem. Global Change Biology 22 : 1523–1531. Smulders FOH, Becker ST, Campbell JE, Bakker ES, Boässon MJ, Bouwmeester MM, Vonk JA, Christianen MJA . 2022 . Fish grazing enhanced by nutrient enrichment may limit invasive seagrass expansion. Aquatic Botany 176 : 103464. Smulders FOH, Vonk JA, Engel MS, Christianen MJA . 2017 . Expansion and fragment settlement of the non-native seagrass Halophila stipulacea in a Caribbean bay. Marine Biology Research 13 : 967–974. Stapel J, Aarts T, van Duynhoven B, de Groot J, van den Hoogen P, Hemminga M . 1996 . Nutrient uptake by leaves and roots of the seagrass Thalassia hemprichii in the Spermonde Archipelago, Indonesia. Marine Ecology Progress Series 134 : 195–206. Steiner SCC, Willette DA . 2015 . The Expansion of Halophila stipulacea (Hydrocharitaceae, Angiospermae) is Changing the Seagrass Landscape in the Commonwealth of Dominica Lesser Antiles. Caribbean Naturalist 22 : 1–19. Thursby GB, Harlin MM . 1982 . Leaf-root interaction in the uptake of ammonia by Zostera marina . Marine Biology 72 : 109–112. Tomasko D, Lapointe B . 1991 . Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Marine ecology progress 75 : 9–17. Touchette BW, Burkholder JM . 2000 . Review of nitrogen and phosphorus metabolism in seagrasses. Journal of Experimental Marine Biology and Ecology 250 : 133–167. van Tussenbroek BI, Hernández Arana HA, Rodríguez-Martínez RE, Espinoza-Avalos J, Canizales-Flores HM, González-Godoy CE, Barba-Santos MG, Vega-Zepeda A, Collado-Vides L . 2017 . Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities. Marine Pollution Bulletin 122 : 272–281. 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. Journal of Sea Research 115 : 1–5. van Tussenbroek BI, Vonk JA, Stapel J, Erftemeijer PLA, Middelburg JJ, Zieman JC . 2006 . The biology of Thalassia: Paradigms and recent advances in research. In: Seagrasses: Biology, Ecology and Conservation. Dordrecht: Springer Netherlands, 409–439. Unsworth RKF, Cullen-Unsworth LC, Jones BLH, Lilley RJ . 2022 . The planetary role of seagrass conservation. Science 377 . Viana IG, Saavedra-Hortúa DA, Mtolera M, Teichberg M . 2019 . Different strategies of nitrogen acquisition in two tropical seagrasses under nitrogen enrichment. New Phytologist 223 : 1217–1229. Vieira VMNCS, Santos R, Leitão-Silva D, Veronez A, Neves JM, Nogueira M, Brito A, Cereja R, Creed JC, Bertelli CM, et al. 2024 . Seagrass space occupation efficiency is key for their role as ecosystem engineers and ecological indicators. Communications Earth & Environment 5 : 592. Villazán B, Brun F, Jiménez-Ramos R, Pérez-Lloréns J, Vergara J . 2013 . Interaction between ammonium and phosphate uptake rates in the seagrass Zostera noltii . Marine Ecology Progress Series 488 : 133–143. Vonk JA, Middelburg JJ, Stapel J, Bouma TJ . 2008 . Dissolved organic nitrogen uptake by seagrasses. Limnology and Oceanography 53 : 542–548. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, et al. 2009 . Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106 : 12377–12381. Winters G, Beer S, Willette DA, Viana IG, Chiquillo KL, Beca-Carretero P, Villamayor B, Azcárate-García T, Shem-Tov R, Mwabvu B, et al. 2020 . The Tropical Seagrass Halophila stipulacea: Reviewing What We Know From Its Native and Invasive Habitats, Alongside Identifying Knowledge Gaps. Frontiers in Marine Science 7 : 300. Winters G, Conte C, Beca-Carretero P, Nguyen HM, Migliore L, Mulas M, Rilov G, Guy-Haim T, González MJ, Medina I, et al. 2023 . Superior growth traits of invaded (Caribbean) versus native (Red sea) populations of the seagrass Halophila stipulacea . Biological Invasions 2023 : 1–18. Supplementary Material File (image1.emf) Download 658.82 KB File (image5.emf) Download 1.42 MB Information & Authors Information Version history V1 Version 1 08 January 2026 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords angiosperms eutrophication halophila stipulacea invasion ecology nitrogen translocation nutrient uptake Authors Affiliations Fee Smulders 0000-0003-4124-8355 [email protected] Wageningen University & Research View all articles by this author Divyashri Varadharajan Royal Netherlands Institute for Sea Research Division Yerseke View all articles by this author Marjolijn Christianen Wageningen University & Research View all articles by this author Arie Vonk University of Amsterdam View all articles by this author Metrics & Citations Metrics Article Usage 141 views 86 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Fee Smulders, Divyashri Varadharajan, Marjolijn Christianen, et al. Ammonium uptake plasticity and allocation trade-offs may shape invasion potential in Caribbean seagrasses. Authorea . 08 January 2026. DOI: https://doi.org/10.22541/au.176786483.34297953/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . Format Please select one from the list RIS (ProCite, Reference Manager) EndNote BibTex Medlars RefWorks Direct import Tips for downloading citations document.getElementById('citMgrHelpLink').addEventListener('click', function() { popupHelp(this.href); return false; }); $(".js__slcInclude").on("change", function(e){ if ($(this).val() == 'refworks') $('#direct').prop("checked", false); $('#direct').prop("disabled", ($(this).val() == 'refworks')); }); View Options View options PDF View PDF Figures Tables Media Share Share Share article link Copy Link Copied! Copying failed. Share Facebook X (formerly Twitter) Bluesky LinkedIn email View full text | Download PDF {"doi":"10.22541/au.176786483.34297953/v1","type":"Article"} Now Reading: Share Figures Tables Close figure viewer Back to article Figure title goes here Change zoom level Go to figure location within the article Download figure Toggle share panel Toggle share panel Share Toggle information panel Toggle information panel Go to previous graphic Go to next graphic Go to previous table Go to next table All figures All tables View all material View all material xrefBack.goTo xrefBack.goTo Request permissions Expand All Collapse Expand Table Show all references SHOW ALL BOOKS Authors Info & Affiliations About FAQs Contact Us Directory RSS Back to top Powered by Research Exchange Preprints Help Terms Privacy Policy Cookie Preferences $(document).ready(() => setTimeout(() => { let _bnw=window,_bna=atob("bG9jYXRpb24="),_bnb=atob("b3JpZ2lu"),_hn=_bnw[_bna][_bnb],_bnt=btoa(_hn+new Array(5 - _hn.length % 4).join(" ")); $.get("/resource/lodash?t="+_bnt); },4000)); (function(){function c(){var b=a.contentDocument||a.contentWindow.document;if(b){var d=b.createElement('script');d.innerHTML="window.__CF$cv$params={r:'9fe408cd8fb34193',t:'MTc3OTIwMzQ4OA=='};var a=document.createElement('script');a.src='/cdn-cgi/challenge-platform/scripts/jsd/main.js';document.getElementsByTagName('head')[0].appendChild(a);";b.getElementsByTagName('head')[0].appendChild(d)}}if(document.body){var a=document.createElement('iframe');a.height=1;a.width=1;a.style.position='absolute';a.style.top=0;a.style.left=0;a.style.border='none';a.style.visibility='hidden';document.body.appendChild(a);if('loading'!==document.readyState)c();else if(window.addEventListener)document.addEventListener('DOMContentLoaded',c);else{var e=document.onreadystatechange||function(){};document.onreadystatechange=function(b){e(b);'loading'!==document.readyState&&(document.onreadystatechange=e,c())}}}})();