Within-population spatial genetic structure in four naturally fragmented species of a neotropical inselberg radiation, Alcantarea imperialis, A. geniculata, A. glaziouana and A. regina (Bromeliaceae)

Studies of organisms on 'terrestrial islands' can improve our understanding of two unresolved issues in evolutionary genetics: the likely long-term effects of habitat fragmentation and the genetic underpinnings of continental species radiations in island-like terrestrial habitats. We have addressed both issues for four closely related plant species of the adaptive radiation Bromeliaceae, Alcantarea imperialis, A. geniculata, A. regina and A. glaziouana. All four are adapted to ancient, isolated inselberg rock outcrops in the Brazilian Atlantic rainforest and are thus long-term fragmented by nature. We used eight nuclear microsatellites to study within-population spatial genetic structure (SGS) and historical gene dispersal in nine populations of these species. Within-population SGS reflected known between-species differences in mating systems. The strongest SGS observed in A. glaziouana (Sp=0.947) was stronger than literature estimates available for plants. Analysis of short- and long-distance components of SGS identified biparental inbreeding, selfing and restricted seed dispersal as main determinants of SGS, with restricted pollen dispersal by bats contributing in some localities. The ability of Alcantarea spp. to colonize isolated inselbergs probably stems from their flexible mating systems and an ability to tolerate inbreeding. Short-ranging gene dispersal (average sigma=7-27 m) is consistent with a loss of dispersal power in terrestrial island habitats. Population subdivision associated with sympatric colour morphs in A. imperialis is accompanied by between-morph differences in pollen and seed dispersal. Our results indicate a high potential for divergence with gene flow in inselberg bromeliads and they provide base-line data about the long-term effects of fragmentation in plants.     

Diversity and ecology of saxicolous vegetation mats on inselbergs in the Brazilian Atlantic rainforest

Inselbergs occur as mostly dome-shaped rock outcrops in all climatic and vegetational zones of the tropics. Consisting of Precambrian granites and gneisses, they form ancient and stable landscape elements. Due to harsh edaphic and microclimatic conditions, the vegetation of inselbergs differs markedly from those of the surroundings. Monocotyledonous mats form one of the most characteristic communities of this ecosystem. The floristic composition of this community was studied on six inselbergs located in the Brazilian Atlantic rainforest. Dominating are Bromeliaceae ( Alcantarea , Encholirium ), Velloziaceae ( Vellozia ), Cactaceae ( Coleocephalocereus ) and the Cyperaceae Trilepis . The alpha diversity of the mats was relatively uniform among the six outcrops. However, beta diversity varied considerably between the different sites. Beta diversity was highest at the most speciose locality indicating a high degree of stochasticity in colonization. In contrast to the low diversity mats on West African inselbergs, the Brazilian rock outcrops bear a floristically more diverse mat community rich in endemics. Thus the edaphically controlled inselberg vegetation reflects the outstanding diversity of the Mata Atlaântica. Possibly the high species richness of mats on East Brazilian inselbergs is a consequence of a large species-pool. The processes that regulate regional and local diversity in the Mata Atlaântica are not fully clear. It is assumed that historical (i.e. long-term stability) and biotic (i.e. evolutionary interchange of taxa between canopies and rock outcrops followed by differentiation of local populations) conditions have promoted high rates of speciation and their coexistence in isolated habitats. A danger to the unique vegetation of East Brazilian inselbergs is the establishment of invasive weeds.     

Sympatric bromeliad species (Pitcairnia spp.) facilitate tests of mechanisms involved in species cohesion and reproductive isolation in Neotropical inselbergs

The roles of intra- and interspecific gene flow in speciation and species evolution are topics of great current interest in molecular ecology and evolutionary biology. Recent modelling studies call for new empirical data to test hypotheses arising from the recent shift from a 'whole-genome reproductive isolation' view to a 'genic' view of species and speciation. Particularly scarce (and thus of particular interest) are molecular genetic data on recently radiated, naturally hybridizing species in strongly structured and species-rich environments. Here, we studied four sympatric plant species (Pitcairnia spp.; Bromeliaceae) adapted to Neotropical inselbergs (isolated outcrops resembling habitat 'islands' in tropical rainforests) using nuclear and plastid DNA. Patterns of plastid DNA haplotype sharing and nuclear genomic admixture suggest the presence of both, incomplete lineage sorting and interspecific gene flow over extended periods of time. Integrity and cohesion of inselberg species of Pitcairnia are maintained despite introgression and in the face of extremely low within-species migration rates (N(e)m < 1 migrant per generation). Cross-evaluation of our genetic data against published pollination experiments indicate that species integrity is maintained by the simultaneous action of multiple prezygotic barriers, including flowering phenology, pollinator isolation and divergent mating systems. Postzygotic Bateson-Dobzhansky-Muller incompatibilities appear to contribute to isolation, as suggested by asymmetric introgression rates of single loci. Our results suggest that incomplete lineage sorting, hybridization and introgression form integral aspects of adaptive radiation in Neotropical inselberg 'archipelagos'. Inselbergs with multiple closely related co-occurring species should be of special interest to students of speciation in mountain systems, and to ongoing conservation programmes in the Atlantic Rainforest biodiversity hotspot.     

Molecular phylogenetics of the Brazilian giant bromeliads (Alcantarea, Bromeliaceae): implications for morphological evolution and biogeography

The genus Alcantarea comprises near 30 species endemic to rocky outcrops from eastern Brazil. Most species are ornamental and several are threatened due to habitat loss and over collection. In this paper we examine the phylogenetics of Alcantarea and its relationship with the Brazilian members of Vriesea, a genus of which Alcantarea has been treated as a subgenus. We discuss the morphological evolution of the stamen position and its implication for pollination and the occurrence of Alcantarea in the Espinha?o mountain range rocky savanna-like habitat vegetation. DNA sequence data derived from two plastid markers (trnK-rps16, trnC-petN) and from a low copy nuclear gene (Floricaula/Leafy) together with 20 nuclear microsatellite loci were the data source to perform analyses and construct phylogenetic and Neighbor Joining trees for the genus. Alcantarea is well supported as monophyletic in both Bayesian and parsimony analyses, but sections of Vriesea, represented by the eastern Brazilian species, appear paraphyletic. Microsatellites delimit geographically isolated species groups. Nevertheless individuals belonging to a single species may appear related to distinct clusters of species, suggesting that hybridization and/or homoplasy and/or incomplete lineage sorting are also influencing the analysis based on such markers and may be the reasons for some unexpected results. Alcantarea brasiliana is hypothesized as putative hybrid between A. imperialis and A. geniculata. Spreading stamens, a morphological floral characteristic assumed to be related to Chiropterophily, apparently evolved multiple times within the genus, and invasion of rocky savanna-like habitat vegetation by Atlantic rainforest ancestors seems to have occurred multiple times as well.     

Alcantarea (Bromeliaceae) leaf anatomical characterization and its systematic implications

Alcantarea (Bromeliaceae) has 26 species that are endemic to eastern Brazil, occurring mainly on gneiss–granitic rock outcrops (‘inselbergs’). Alcantarea has great ornamental potential and several species are cultivated in gardens. Limited data is available in the literature regarding the leaf anatomical features of the genus, though it has been shown that it may provide valuable information for characterizing of Bromeliaceae taxa. In the present work, we employed leaf anatomy to better characterize the genus and understand its radiation into harsh environments, such as inselbergs. We also searched for characteristics potentially useful in phylogenetic analyses and in delimiting Alcantarea and Vriesea. The anatomical features of the leaves, observed for various Alcantarea species, are in accordance with the general pattern shown by other Bromeliaceae members. However, some features are notable for their importance for sustaining life on rock outcrops, such as: small epidermal thick‐walled cells, uneven sinuous epidermal walls, hypodermis often differentiated into lignified layers with thick‐walled cells, aquiferous hypodermis bearing collapsible cells, and the presence of well developed epicuticular stratum. Alcantarea leaves tend to show different shapes in the spongy parenchyma, and have chlorenchymatous palisade parenchyma arranged in more well‐defined arches, when compared to Vriesea species from the same habitat.     

Biodiversity and vegetation of small-sized inselbergs in a West African rain forest (Taı, Ivory Coast)

The vegetation of small granitic rock outcrops (geomorphologically small-sized inselbergs) which do not reach the canopy was studied in the Taı rain forest (southwestern Ivory Coast) under aspects of species diversity and phytogeographical affinities. Rock outcrops form edaphically arid (due to absent or very sparse soil cover) and microclimatologically xeric (i.e. low air humidity, temperature regularly exceeding 50°C) islands with cryptogamic crusts, succulents and poikilohydric vascular plants as characteristic elements of their vegetation which differs totally from the surrounding forest. Altogether sixty-six species of vascular plants out of twenty-nine families occur, the number of species correlates positively with inselberg size. Compared with large inselbergs the microclimatic attributes of small-sized rock outcrops are less pronounced. This is accompanied by a decrease of typical inselberg taxa (i.e. species mainly occurring on inselbergs). Low beta diversity between inselbergs indicates deterministic influences as important regulators of species composition. Annual Poaceae and Cyperaceae are richly represented. It can be hypothesized that inselbergs may represent natural growing sites of widely distributed tropical weeds today. Inselbergs might provide habitat resources for savanna elements in rain forest zones.     

A set of polymorphic microsatellite loci for Vriesea gigantea and Alcantarea imperialis (Bromeliaceae) and cross‐amplification in other bromeliad species

Fifteen polymorphic microsatellite markers were isolated and characterized in two species of Bromeliaceae: Vriesea gigantea and Alcantarea imperialis. The number of alleles observed for each locus ranged from three to 16. The loci will be used for studies of the genetic structure of natural populations, reproductive biology, and evolutionary relationships among and within these genera. A cross‐amplification test in 22 taxa suggests that the markers will be useful for similar applications in numerous other bromeliad species.     

Genetic relationships and variation in reproductive strategies in four closely related bromeliads adapted to neotropical 'inselbergs': Alcantarea glaziouana, A. regina, A. geniculata and A. imperialis (Bromeliaceae)

Background and Aims: Bromeliads (Bromeliaceae) adapted to rock outcrops or ‘inselbergs’in neotropical rain forests have been identified as suitableplant models for studying population divergence and speciationduring continental plant radiations. Little is known about geneticrelationships and variation in reproductive strategies withinand among inselberg-adapted species, yet knowledge of theseparameters is important for understanding divergence processesand for conservation planning. Methods: Nuclear microsatellites were used to assess the role of clonalreproduction, estimate genetic diversity and explore geneticrelationships and variation in reproductive strategies for atotal of 15 populations of four closely related Alcantarea inselbergspecies in south-eastern Brazil: A. glaziouana, A. regina, A.geniculata and A. imperialis. Key Results: Clonal propagation is frequent in coastal populations of A.glaziouana and A. regina, but absent in the high-altitude speciesA. geniculata and A. imperialis. Considerable variation in clonaldiversity, gene diversity (H_e), allelic richness, and Wright'sinbreeding coefficient (F_IS) exists within and between speciesof Alcantarea. A Bayesian analysis of coastal inselberg speciesindicated pronounced genetic structure. A neighbor-joining analysisgrouped populations of each species together with moderate bootstrapsupport, except for the high altitude species A. imperialis. Conclusions: The coastal inselberg species A. glaziouana and A. regina tendto propagate asexually via vegetative clonal growth, and bothreproductive strategies and breeding systems vary greatly betweenpopulations and species of Alcantarea. The microsatellite dataindicate a history of hybridization and reticulation involvingthe high-altitude species A. geniculata and A. imperialis inareas of co-occurrence. The results highlight the need to understandsimilarities and differences in reproductive strategies bothwithin and between related species for conservation planningand as a basis for understanding evolutionary processes in tropicalradiations.     

Molecular ecology studies of species radiations: current research gaps,opportunities and challenges

Understanding the drivers and limits of species radiations is a crucial goal of evolutionary genetics and molecular ecology, yet research on this topic has been hampered by the notorious difficulty of connecting micro‐ and macroevolutionary approaches to studying the drivers of diversification. To chart the current research gaps, opportunities and challenges of molecular ecology approaches to studying radiations, we examine the literature in the journal Molecular Ecology and revisit recent high‐profile examples of evolutionary genomic research on radiations. We find that available studies of radiations are highly unevenly distributed among taxa, with many ecologically important and species‐rich organismal groups remaining severely understudied, including arthropods, plants and fungi. Most studies employed molecular methods suitable over either short or long evolutionary time scales, such as microsatellites or restriction site‐associated DNA sequencing (RAD‐seq) in the former case and conventional amplicon sequencing of organellar DNA in the latter. The potential of molecular ecology studies to address and resolve patterns and processes around the species level in radiating groups of taxa is currently limited primarily by sample size and a dearth of information on radiating nuclear genomes as opposed to organellar ones. Based on our literature survey and personal experience, we suggest possible ways forward in the coming years. We touch on the potential and current limitations of whole‐genome sequencing (WGS) in studies of radiations. We suggest that WGS and targeted (‘capture’) resequencing emerge as the methods of choice for scaling up the sampling of populations, species and genomes, including currently understudied organismal groups and the genes or regulatory elements expected to matter most to species radiations.     

Influences of gene flow on adaptive speciation in the Dubautia arborea--D. ciliolata complex

Mechanisms of reproductive isolation during plant speciation are often unclear because distinct species often experience high levels of gene flow and hybridization. Adaptive radiations such as the Hawaiian silversword alliance (HSA) provide unique opportunities to study the interactions of selection, gene flow and isolating mechanisms during the speciation process. We examined patterns of phenotypic and genetic differentiation in Dubautia arborea and Dubautia ciliolata, two parapatric HSA taxa that show marked morphological divergence but evidence of weak molecular differentiation, in order to estimate genome-wide differentiation and gene flow patterns. We scored 166 amplified fragment length polymorphism markers in a set of 89 plants from two populations each of D. arborea and D. ciliolata and phenotypically D. arborea-like and D. ciliolata-like plants from a natural hybrid zone. Analyses of population subdivision showed low levels of differentiation between the two species (F(ST) = 0.089) and evidence that the phenotypically parental hybrid zone plants were largely of parental species rather than of hybrid origin. A Bayesian analysis of population ancestry identified a number of plants with admixed D. arborea and D. ciliolata ancestry, even in nonhybrid-zone populations. These results suggest that genome-wide low levels of differentiation between D. arborea and D. ciliolata are in part due to gene flow, and favour models of genic speciation and collective evolution in which gene flow has different effects on selected loci vs. nonselected genomic regions. We discuss ecological and climatic factors that may have shaped patterns of differentiation in this species complex.     

Ecology and Distribution of Melastomataceae in African Rain Forest Inselbergs1

The ecology and distribution of thirty‐seven Melastomataceae species found on 29 inselbergs in the rain forest of Equatorial Guinea, Gabon, and Cameroon are described. The relative contributions of climatic determinism, and stochastic and historical processes to the present distribution of the species amongst the study sites are investigated. Inselbergs are rock outcrops enduring very harsh edaphic and microclimatic conditions, forming “xeric islands” in the rain forest, where natural grasslands develop. For each Melastomataceae species, the habitats where they were collected on the inselbergs and in other biotopes were listed, and their phytogeographical distribution was established. Three species are restricted to rock outcrops. Most species are distributed inside the Guineo‐Congolian Region. Three species have disjunct distributions on rain forest inselbergs and have their main distribution area outside the forested zone. The distribution of the species amongst the inselbergs is correlated to the altitude and the annual rainfall of the sites, and to inselberg geographical location. This correlation of the species distribution with the geographical location of the inselberg is attributed to the spatial autocorrelation of environmental variables and to the combined effects of the history of past vegetation changes due to climatic fluctuations and dispersal limitation.     

Conservation assessment of an extremely restricted bromeliad highlights the need for population-based conservation on granitic inselbergs of the Brazilian Atlantic Forest

Inselbergs support highly specialized vegetation with many endemic species. Here we studied by an integrated approach a rare and threatened species from Brazilian inselbergs. Pitcairnia encholirioides (Bromeliaceae) is included in the Red Book of Brazilian Flora, in the ‘Endangered’ category. Only one single population on unprotected private property was known at the beginning of our study. We studied several life-history traits including clonal growth, reproductive biology, seed germination and cryopreservation, and genetic diversity. Pitcairnia encholirioides has the phalanx type of clonal growth strategy. Its self-incompatible flowers are successfully pollinated by hummingbirds. However, less than 5% of clonal fragments produced flowers. Seeds can be wind-dispersed, but most of them are dispersed by gravity and fall close to the mother plant. The percentage and speed of germination were significantly affected by different temperatures, water potential, and red:far-red light ratios, although more than 80% of seeds germinated under optimal physiological conditions. The genetic diversity was very low (H_sp = 0.09) and the population was highly structured (Φ_ST = 0.51). The combination of dispersal mode and environmental conditions seems to be the main factor leading to the rarity of P. encholiroides. Low genetic diversity combined with small population size and low reproductive capacity suggest that the species is highly susceptible to environmental disturbance. Similarly to P. encholiroides, many species from Brazilian inselbergs are restricted to only a few localities. For more widely distributed species, a higher genetic diversity among populations has been consistently detected. The pattern of low gene flow of many species with small distributions highlight the importance of population-based conservation strategies for such taxa the areas of occurrence of which being naturally fragmented at inselberg sites. We discuss some strategies that may help in conservation of such species.     

Three fundamental contributions of molecular genetics to avian ecology and evolution

Studies in molecular genetics are having revisionary impact in at least three broad areas of avian ecology and evolution: mating systems, geographic population structure and gene flow, and phylogenetic relationships among species and higher taxa. With regard to mating systems, genetic analyses of maternity and paternity have revealed unexpectedly high frequencies of extra-pair fertilization and intraspecific brood parasitism in numerous avian species (including those thought to be socially monogamous), and these discoveries are prompting a fundamental reshaping of mating system theory for birds. With regard to genetic structure, molecular markers have uncovered a great variety of depths and patterns in the phylogeographic histories of conspecific populations, and these findings provide novel perspectives on historical gene flow regimes and species concepts. With regard to evolutionary relationships among higher avian taxa, molecular findings have suggested several phylogenetic realignments, thus prompting renewed interest in the cross-comparative aspects of molecular and morphological evolution as well as of alternative procedures for molecular analysis.     

Three fundamental contributions of molecular genetics to avian ecology and evolution

Studies in molecular genetics are having revisionary impact in at least three broad areas of avian ecology and evolution: mating systems, geographic population structure and gene flow, and phylogenetic relationships among species and higher taxa. With regard to mating systems, genetic analyses of maternity and paternity have revealed unexpectedly high frequencies of extra-pair fertilization and intraspecific brood parasitism in numerous avian species (including those thought to be socially monogamous), and these discoveries are prompting a fundamental reshaping of mating system theory for birds. With regard to genetic structure, molecular markers have uncovered a great variety of depths and patterns in the phylogeographic histories of conspecific populations, and these findings provide novel perspectives on historical gene flow regimes and species concepts. With regard to evolutionary relationships among higher avian taxa, molecular findings have suggested several phylogenetic realignments, thus prompting renewed interest in the cross-comparative aspects of molecular and morphological evolution as well as of alternative procedures for molecular analysis.     

Island–matrix relationships in Nama Karoo inselberg landscapes. Part I: Do inselbergs provide a refuge for matrix species?

In a first step to investigate the potential source-sink functionof isolated mountains (i.e. inselbergs) in an arid landscape,affinities of inselberg floras with their surrounding were investigated in foursets of inselbergs in Namibia's Nama Karoo. The questions focussed on(a) the potential of inselbergs to serve as sources for degradedrangelands, and (b) the role of species attributes in the relationshipbetween inselberg and matrix. The study showed that inselbergs can serve assource for degraded rangeland, but at regional and landscape level employed inthis analysis, the species attributes growth form and seed dispersal did notprovide any conclusive trends.     

Bromeliaceae diversity and conservation in Minas Gerais state,Brazil

Field work and data from herbaria collections (2686 records) representing 283 taxa (265 species and 18 infraspecific taxa) of Bromeliaceae occurring at Minas Gerais state, southeastern Brazil, were analyzed in order to obtain distribution and diversity information, and to determine IUCN (The World Conservation Union) conservation status for each taxon. A map containing 1° × 1° grid cells was used to identify priority areas for new research collections, areas of high species diversity, and Bromeliaceae conservation status. A clear decrease in Bromeliaceae diversity is observed between the eastern and the western portions of Minas Gerais, and low floristic similarities were found between neighboring grid cells. The rocky mountains of Cadeia do Espinhaço are considered the most important area for Bromeliaceae endemics. From the 283 taxa of Bromeliaceae that occur at Minas Gerais, 118 (42%) are considered threatened, and 124 taxa (44% of the total) do not occur inside any protected area. The region of the Quadrilátero Ferrífero in the southern portion of the Cadeia do Espinhaço is the most threatened, and urgent strategies for conservation of this rich Bromeliaceae flora are needed. Northeastern Minas Gerais, particularly the rocky outcrops or inselbergs located in the Jequitinhonha and Mucuri rivers drainage basins need additional collection efforts and conservation actions focused on these saxicolous taxa.     

Genetic structure of the saxicole Pitcairnia geyskesii (Bromeliaceae) on inselbergs in French Guiana

South American inselbergs constitute singular and fragmented habitats in the tropical rain forest. Pitcairnia geyskesii is restricted to these habitats and exhibits both sexual and asexual reproduction. The genetic structure of populations on three inselbergs in French Guiana is examined by analysis of ten isozyme loci. All analyzed populations show high levels of genetic variation. On average, 63.3% of loci per population were polymorphic, with a mean number of 2.21 alleles per polymorphic locus, and mean observed and expected heterozygosities of 0.185 and 0.183, respectively. The analyses of genetic variability displayed at different levels (inselbergs, subpopulations, and mats) give different but complementary information. A significant multilocus disequilibrium was detected in one subpopulation, whereas none was observed within the whole populations sampled on the three inselbergs. Tests on spatial genetic structure indicate a patchy distribution of genotypes on two inselbergs. The data give some insights on the reproductive behavior of P. geyskesii. (1) Efficient sexual reproduction leads to seed recruitment at the level of the inselberg. (2) Both clonality and seed recruitment occur within mats. (3) Vegetative spread by fragmentation is involved in the establishment of new mats. There is substantial differentiation (F(ST) = 0.322) and low gene flow among inselbergs (Nm = 0.234). High genetic diversity within inselbergs appears as a consequence of the association of genet longevity induced by clonal replication and recruitment of new genets produced by sexual reproduction.     

Integrating floral scent, pollination ecology and population genetics

1 . Floral scent is a key factor in the attraction of pollinators. Despite this, the role of floral scent in angiosperm speciation and evolution remains poorly understood. Modern population genetic approaches when combined with pollination ecology can open new opportunities for studying the evolutionary role of floral scent.
2 . A framework of six hypotheses for the application of population genetic tools to questions about the evolutionary role of floral scent is presented. When floral volatile chemistry is linked to pollinator attraction we can analyse questions such as: Does floral volatile composition reflect plant species boundaries? Can floral scent facilitate or suppress hybridization between taxa? Can the attraction of different pollinators influence plant mating systems and pollen-mediated gene flow? How is population genetic structure indirectly influenced by floral scent variation?
3 . The application of molecular tools in sexually deceptive orchids has confirmed that volatile composition reflects species boundaries, revealed the role of shared floral odour in enabling hybridization, confirmed that the sexual attraction mediated by floral odour has implications for pollen flow and population genetic structure and provided examples of pollinator-mediated selection on floral scent variation. Interdisciplinary studies to explore links between floral volatile variation, ecology and population genetics are rare in other plant groups.
4 . Ideal study systems for future floral scent research that incorporate population genetics will include closely related taxa that are morphologically similar, sympatric and co-flowering as well as groups that display wide variation in pollination mechanisms and floral volatiles.     

居群遗传学原理及其在珍稀濒危植物保护中的应用

居群遗传学在珍稀濒危植物保护研究中有着重要的应用价值。本文首先介绍了居群遗传学中的几个重要概念——有效居群大小、近交繁殖、遗传漂变和基因流,然后详细叙述了居群遗传学原理在珍稀濒危植物保护中的应用途径和前景。     

红树植物分子生态与进化研究进展

红树林是热带与亚热带海洋森林和地球湿地生态系统的重要组成部分 ,是多种海洋动物及鸟类栖息繁衍的重要场所 ,在调节全球生态平衡及维持生物多样性方面起着十分重要的作用。有关红树林的生态生物学研究 ,特别是红树林及其生物多样性变化的监测研究 ,红树林的保护与管理已成为热带亚热带海洋及湿地生态学研究的重要内容。海南岛有长达 1 5 2 8ｋｍ的海岸线 ,红树林群落的分布十分广泛。孢粉学证据说明 ,海南岛滨海地区在第三纪时即有红树林出现[1 ] 。现海南岛红树林植物种类有 1 8科 2 6属 34种 ,占中国红树植物种数的 97.1 % [2 ] 。由于…