A resilience dichotomy in mangrove forests: Native resistance versus exotic compensation to climatic and tidal extremes

During community assembly, early arriving exotic species might suppress other species to a greater extent than do native species. Because most exotics were intentionally introduced, we hypothesize there was human selection on regeneration traits during introduction. This could have occurred at the across- or within-species level (e.g. during cultivar development). We tested these predictions by seeding a single species that was either native, exotic 'wild-type' (from their native range), or exotic 'cultivated' using 28 grassland species in a glasshouse experiment. Priority effects were assessed by measuring species' effect on establishment of species from a seed mix added 21 d later. Exotic species had higher germination and earlier emergence dates than native species, and differences were found in both 'wild' and 'cultivated' exotics. Exotic species reduced biomass and species diversity of later arriving species much more than native species, regardless of seed source. Results indicate that in situations in which priority effects are likely to be strong, effects will be greater when an exotic species arrives first than when a native species arrives first; and this difference is not merely a result of exotic species cultivation, but might be a general native-exotic difference that deserves further study.

Ecosystem dynamics and the responses to climate change in mangrove forests are poorly understood. We applied the biogeochemical process model Biome-BGC to simulate the dynamics of net primary productivity (NPP) and leaf area index (LAI) under the present and future climate conditions in mangrove forests in Shenzhen, Zhanjiang, and Qiongshan across the southern coast of China, and in three monocultural mangrove stands of two native species, Avicennia marina and Kandelia obovata, and one exotic species, Sonneratia apetala, in Shenzhen. The soil hydrological process of the model was modified by incorporating a soil water (SW) stress index to account for the impact of the effective SW availability in the coastal wetland. Our modified Biome-BGC well predicted the dynamics of NPP and LAI in the mangrove forests at the study sites. We found that the six mangrove systems differed in sensitivity to variations in the effective SW availability. At the ecosystem level, however, soil salinity alone could not entirely explain the limitation of the effective SW availability on the productivity of mangrove forests. Increasing atmospheric CO2 concentration differentially affected growth of different mangrove species but only had a small impact on NPP (<7%); whereas a doubling of atmospheric CO2 concentration associated with a 2°C temperature rise would increase NPP by 14–19% across the three geographically separate mangrove forests and by 12% to as much as 68% across the three monocultural mangrove stands. Our simulation analysis indicates that temperature change is more important than increasing CO2 concentration in affecting productivity of mangroves at the ecosystem level, and that different mangrove species differ in sensitivity to increases in temperature and CO2 concentration.

Exotic fast-growing tree species have been commonly planted as pioneer species to facilitate ecological restoration in South China. Their growth and resource utilization behavior related to intrinsic physiology and structural properties have profound influences on forest ecosystem. However, the contrastive research focusing on water utilization features along with xylem anatomical properties between native and exotic species is scarce in South China. The objective of this study is to investigate the sapwood anatomical characteristics and water utilization conditions of native and exotic fast-growing species, and to elucidate the relationship between sap-flux density and conduit features. We measured sap-flux density, conduit length, diameter and density of four native species (Schima superba, Michelia macclurei, Castanopsis hystrix and Castanopsis fissa) and four exotic species (Eucalyptus citriodora, Eucalyptus urophylla × grandis, Acacia auriculaeformis and Acacia mangium). Sap flux density was measured based on the Granier’s thermal dissipation probe method. The whole-tree water transport was quantified by multiplying sap-flux density by sapwood area. The measurements of conduit characteristics were conducted by using segregation and slice method. Sapwood area increased with the growing diameter at breast height (DBH) as a power function. Native species had a larger water-conducting tissue area than exotic species at the same DBH value when trees grew to a size with a certain value of DBH. The conduit diameter of exotic species was significantly larger than that of native species. Conversely, native species, such as S. superba and M. macclurei, had longer conduit length and higher conduit density than other tree species. Based on a physiological interpretation of the measured conduit characteristics, native tree species developed a safe water transport system while exotic fast-growing tree species come into being an efficient system instead. Water transport increased with the growing DBH as a power function, and the exponent for native species (1.60) was higher than that for exotic species (1.22). Under the combined impact of sap-flux density and sapwood area, native species presented a larger water transport at a larger DBH value, indicating that growth advantage of exotic fast-growing species might weaken as DBH increased.

To rapidly rehabilitate mangrove forests, exotic mangrove species characterized by high growth rates have been introduced in China, which would undoubtedly affect the nutrient status, nutrient acquisition and utilization strategies of mangrove plants, but the mechanism remains unclear. Qi’ao Island (a suburb of Zhuhai City) has the largest continuous exotic mangrove forests in China, where a mass collection of mangrove soils, plant tissues and tidewater was conducted. Ecological stoichiometric ratios and isotopic compositions were then analyzed to evaluate the ecosystem-scale nutrient status and compare the nutrient acquisition and utilization strategies of native Kandelia obovata (KO) and exotic Sonneratia apetala (SA) species. Soil and foliar C:N:P stoichiometries indicated that there is high P availability but N limitations, while further isotopic evidence indicated that native KO and exotic SA responded differently to the N limitation status. First, native KO seemed to prefer NO3−, while exotic SA preferred NH4+, according to the Δ15Nleaf–root (leaf–root δ15N difference) as well as the relationships between foliar δ15N and soil-extracted NH4+ δ15N, and between N and heavy metal contents. This suggested possible inter-specific competition between native KO and exotic SA, leading to different N species’ preferences to maximize resource utilization. Next, native KO likely adopted the “conservative” strategy to ensure survival with reduced investment in N-rich growth components but root systems leading to lower growth rates and higher N use efficiency (NUE) and intrinsic water use efficiency (iWUE), while exotic SA adopted the “aggressive” strategy to ensure fast growth with heavy investment in N-rich growth components, leading to rapid growth and lower NUE and iWUE, and showing signs of invasiveness. Further, native KO is more responsive to aggravated N limitation by enhancing NUE. This study will provide insights into the adaptation of different mangrove species to nutrient limitations and the risks associated with large-scale plantations of exotic mangrove species.

Light and competition alter leaf stoichiometry of introduced species and native mangrove species

Litterfall may facilitate the outperformance of exotic species by inducing better resource acquisition and reproductive performance. However, the drivers that determine litterfall patterns in exotic and native species have remained insufficiently investigated due to the lack of long-term observations. Here, we employed empirical dynamic modeling on a two-decade-long litterfall observation (1999–2019) in a subtropical mangrove forest in Shenzhen, China, to evaluate the relative importance of environmental drivers on different species. We found that mangrove leaf litterfall in both exotic and native species was strongly altered by temperature, and the causal relationship was stronger in the dominant exotic species Sonneratia apetala compared to native species. However, the main driver of reproductive output differed largely between exotic and native species; temperature was the main cause of native reproduction, whereas coastal nutrients drove the reproductive output of exotic species. Our study highlighted that high nutrient availability in Shenzhen Bay in the past decade allowed the exotic species S. apetala to gain better reproductive output than native species. We imply that enriched nutrients in coastal water likely contributed to exotic dominance in China’s coastal mangrove forest.

Semi-arid regions with Mediterranean-type climates harbor exceptional biodiversity, but are increasingly threatened by invading exotic annual species and climatic changes, including drought. In semi-arid ecosystems, antecedent conditions often influence plant growth, but the role of antecedent conditions for drought response and recovery of native versus exotic species remains largely unexplored. From 2013 to 2016, we imposed experimental rainfall treatments (average rainfall, moderate or severe drought) in plots under a native shrub canopy and in inter-spaces dominated by herbaceous vegetation, and quantified growth (peak biomass) and abundance (cover) of native and exotic herbaceous species. The following year, we quantified recovery from the drought treatments (2017). Exotic biomass was less resistant to drought (declined more than native biomass), but was more resilient (increased more than native biomass in the year following drought), especially in unshaded inter-spaces between shrubs. These responses were associated with life history; annual species responded more negatively to drought in the inter-spaces than perennial species. Current years' rainfall was a better predictor of biomass than prior rainfall, but antecedent factors were also important. After four years of rainfall treatments, exotic species had the highest growth recovery in the severe drought treatment, while growth of natives had the opposite response. In contrast, litter was positively associated with plant growth regardless of origin. This study demonstrates that when native and exotic species differ in life history, as they do in Mediterranean climate ecosystems, they may respond differently to antecedent factors, and hence differ in recovery from climate extremes such as drought.

In this study, we compared stand structure, biomass and soil carbon pools, and litterfall production between a mixed mangrove forest consisting of Aegiceras corniculatum inter-planted with the exotic Sonneratia apetala and a native monospecific forest dominated by A. corniculatum in the intertidal area of Zhanjiang, Guangdong Province, southeast China. The goal of this study was to test the hypothesis that inter-planting fast growing exotic mangrove S. apetala into subtropical native mangrove forests will significantly increase C sequestration. Although the tree heights and basal diameters of S. apetala were significantly higher than those of A. corniculatum, the density of the 12-year-old S. apetala trees in the mixed forest was much smaller than that of A. corniculatum in the monospecific forest. In contrast to several previous studies on S. apetala forests planted directly on mangrove-free mudflats, the mixed mangrove forest showed no significant difference in either standing biomass or soil carbon pools from the native monospecific mangrove forest (p = 0.294 and 0.073, respectively) twelve years after inter-planting with S. apetala. Moreover, carbon cycling was likely speeded up after inter-planting S. apetala due to higher litterfall input and lower C/N ratio. Thus, inter-planting fast-growing S. apetala into native mangrove forest is not an effective way to increase carbon sequestration in this subtropical mangrove forest. Given that exotic plant species may exert negative impact on native mangrove species and related epifauna, this fast-growing mangrove species is not suitable for mangrove plantation projects aiming mainly at enhancing carbon sequestration.

Trait divergence and the ecosystem impacts of invading species

Invited article: The impacts of non‐native species: a review of the British Ornithologists’ Union's Autumn 2008 Scientific Meeting

Comparison of resistance to pest infestation between native and exotic mangrove species

Quantitative integration of factors that potentially affect exotic species richness and abundance at multiple spatial scales is relatively scarce in the literature. Our aim was to address this gap by evaluating the relative importance of the biotic community, abiotic factors, and landscape characteristics on the establishment and spread of native and exotic plant species. We assessed the effect of these factors on exotic and native species richness and abundance, and used regression tree and variation partitioning analyses to evaluate how these predictors interact to favor or limit exotic and/or native species. We found that landscape filters were especially important for the arrival of both native and exotic species, whereas biotic factors seemed to regulate the abundance of plant species once they were present within the system. However, the combined effects of different types of predictors explained the largest fraction of total variation in all models regarding exotic species. Furthermore, significant predictor variables had opposite effects on native versus exotic species at both local and landscape scales, which suggests that some ecosystem properties affect native and exotic species differently. Exotic species richness and abundance were increased by low values of native species cover and diversity, high landscape heterogeneity and edge density, human disturbances (e.g., mowing and soil disruption), land use activities (e.g., developed and agricultural areas), and proximity to transportation systems, especially highways. However, exotic species were less common in areas with low anthropogenic disturbance, where natural disturbances seemed to favor native plant species.

Light condition and neighbor effects are important environmental factors that need to be considered for restoration of mangroves, especially when introduced species are mixed with native species. To evaluate different mangrove species performance under various light intensities and different planting systems, we selected three native mangrove species (Avicennia marina,Aegiceras corniculatum, andKandelia obovata) and grew them withSonneratia apetalain multispecies plots and in monospecies plots withoutS. apetalaunder three light conditions in Futian Nature Reserve, south China. After 10 months of the experiment, plant functional traits were measured. The results showed thatS. apetalawas a light‐demanding species andA. corniculatumandA. marinawere suitable for growth under the medium light condition. The native species were inhibited byS. apetala. Specifically, the height and basal diameter of the native species were lower in the multispecies plots than in the monospecies plots. In the multispecies plots, native species changed their functional growth traits, with higher‐specific leaf area and chlorophyll content, and reduced leaf thickness, leaf dry‐mass content, and carotenoid content compared to those in the monospecies plots. These results indicated trade‐offs between traits that enhance light interception and traits that stimulate plant growth in native species. Our findings revealed thatS. apetalais an adequate species with good invasion capability for restoration in open‐degraded areas, but its ecological impact on the inhibited growth of native species should be carefully considered in mangrove restoration.

Networks of protected areas are fundamental for biodiversity conservation, but many factors determine their conservation efficiency. In particular, on top of other human-driven disturbances, invasions by non-native species can cause habitat and biodiversity loss. Jointly understanding what drives patterns of plant diversity and of non-native species in protected areas is therefore a priority. We tested whether the richness and composition of native and non-native plant species within a network of protected areas follow similar patterns across spatial scales. Specifically, we addressed three questions: (a) what is the degree of congruence in species richness between native and non-native species? (b) do changes in the composition of non-native species across ecological gradients reflect a similar turnover of native species along the same gradients ? (c) what are the main environmental and human disturbance drivers controlling species richness in these two groups of species? Species richness and composition of native and non-native plant species were compared at two spatial scales: the plot scale (10 m × 10 m) and the Protected Area scale (PA). In addition, we fit Generalized Linear Models to identify the most important drivers of native and non-native species richness at each scale, focusing on environmental conditions (climate, topography) and on the main sources of human disturbance in the area (land use and roads). We found a significant positive correlation between the turnover of native and non-native species composition at both plot and PA scales, whereas their species richness was only correlated at the larger PA scale. The lack of congruence between the richness of native and non-native species at the plot scale was likely driven by differential responses to fine scale environmental factors, with non-natives favoring drier climates and milder slopes (climate and slope). In addition, more non-native species were found closer to road-ways in the reserve network. In contrast, the congruence in the richness of native and non-native species at the broader PA scale was mainly driven by the common influence of PA area, but also by similar responses of the two groups of species to climatic heterogeneity. Thus, our study highlights the strong spatial dependence of the relationship between native and non-native species richness and of their responses to environmental variation. Taken together, our results suggest that within the study region the introduction and establishment of non-native species would be more likely in warmer and dryer areas, with high native species richness at large spatial scale but intermediate levels of anthropogenic disturbances and mild slope inclinations and elevation at fine scale. Such an exhaustive understanding of the factors that influence the spread of non-native species, especially in networks of protected areas is crucial to inform conservation managers on how to control or curb non-native species.

Invasion of native ecosystems by exotic species can seriously threaten native biodiversity, alter ecosystem function, and inhibit conservation. Moreover, restoration of native plant communities is often impeded by competition from exotic species. Exotic species invasion may be limited by unfavorable abiotic conditions and by competition with native species, but the relative importance of biotic and abiotic factors remains controversial and may vary during the invasion process. We used a long-term experiment involving restored vernal pool plant communities to characterize the temporal dynamics of exotic species invasion, and to evaluate the relative support for biotic and abiotic factors affecting invasion resistance. Experimental pools (n=256) were divided among controls and several seeding treatments. In most treatments, native vernal pool species were initially more abundant than exotic species, and pools that initially received more native seeds exhibited lower frequencies of exotic species over time. However, even densely seeded pools were eventually dominated by exotic species, following extreme climatic events that reduced both native and exotic plant densities across the study site. By the sixth year of the experiment, most pools supported more exotics than native vernal pool species, regardless of seeding treatment or pool depth. Although deeper pools were less invaded by exotic species, two exotics (Hordeum marinum and Lolium multiflorum) were able to colonize deeper pools as soon as the cover of native species was reduced by climatic extremes. Based on an information-theoretic analysis, the best model of invasion resistance included a nonlinear effect of seeding treatment and both linear and nonlinear effects of pool depth. Pool depth received more support as a predictor of invasion resistance, but seeding intensity was also strongly supported in multivariate models of invasion, and was the best predictor of resistance to invasion by H. marinum and L. multilorum. We conclude that extreme climatic events can facilitate exotic species invasions by both reducing abiotic constraints and weakening biotic resistance to invasion.