Next Article in Journal
Electrocoagulation as a Remedial Approach for Phosphorus Removal from Onsite Wastewater: A Review
Previous Article in Journal
Mathematical Approach for Directly Solving Air–Water Interfaces in Water Emptying Processes
Previous Article in Special Issue
Heavy Metal Concentrations in Wild and Cultured Oplegnathus fasciatus from the East China Sea and Associated Health Risks
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Water
Volume 16
Issue 22
10.3390/w16223207
water-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Variation in Annual Ring and Wood Anatomy of Six Tree Mangrove Species in the Nicoya Gulf of Costa Rica

by
Róger Moya
1,*,
Carolina Tenorio
1,
Danilo Torres-Gómez
2 and
Miguel Cifuentes-Jara
2,3
1
Escuela de Ingeniería Forestal, Instituto Tecnológico de Costa Rica, Cartago 30109, Costa Rica
2
CATIE-Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba 30501, Costa Rica
3
Smithsonian Environmental Research Institute, Edgewater, MD 21037, USA
*
Author to whom correspondence should be addressed.
Water 2024, 16(22), 3207; https://doi.org/10.3390/w16223207
Submission received: 14 October 2024 / Revised: 27 October 2024 / Accepted: 5 November 2024 / Published: 8 November 2024
(This article belongs to the Special Issue Coastal Ecology and Fisheries Management)
Browse Figures
Versions Notes

Abstract

:
There is limited information regarding the adaptation of anatomical features and growth ring formation to ecological site conditions in Costa Rican mangrove trees. We used the methods and principles of ecological anatomy to explore the relationship between wood properties (e.g., ring formation, anatomical characteristics) and ecological factors for six mangrove tree species growing in three sites in the Gulf of Nicoya in Costa Rica. We found that variations of ecological conditions affected the growth ring formation of Avicennia bicolor, Avicennia germinans, Pelliciera rhizophorae and two species of Rhizophora but not Laguncularia racemosa. Site conditions affected the anatomical features of the mangrove tree species. Ray dimensions (height and width) were the factors most affected, which were followed by the frequency, diameter, and length of vessels. The fiber dimensions, green density, specific gravity, and carbon content were also affected by the site conditions. The plasticity in ray (increasing of ray dimension) and vessel elements (multiple vessels) facilitate efficient hydraulic conductivity amidst negative growth conditions and physiological restrictions for mangrove trees. We hypothesize that soil salinity, freshwater inputs and intertidal flooding influence these changes. Laguncularia racemosa presented the most changes in anatomical features across the different sites, followed by Pelliciera rhizophorae, with identical changes between Avicennia and Rhizophora spp. Finally, site salinity and wave energy affected the highest number of anatomical changes in mangrove tree species, including 38 changes in the wood structures in site 1.

1. Introduction

Mangroves are ecosystems composed of salinity-tolerant plant species growing in tropical and subtropical areas, especially between latitudes 24.0° N and 38.0° S [1]. Mangrove trees have specific morphological and physiological adaptations, which allow for their growth in conditions with high salinity [2]. Globally, mangroves provide numerous very important benefits such as coastal protection against storm surges and tsunamis through wave attenuation, fisheries, new land formation, nurseries and breeding grounds for marine organisms, ecotourism [3], and sustainable human livelihoods [4]. Importantly, in recent years, they have been considered for their high carbon capture potential [5].
The mangrove area in Costa Rica reaches 52,802 ha [6]; 99.85% of it is located along the Pacific coast (Figure 1a). The presence of estuaries, gulfs, and inlets provides optimal habitats for mangrove development and results in a high diversity and structural complexity of mangrove ecosystems [7]. There are three types of canopy structures along the Pacific Coast. (i) Northern-most mangrove ecosystems are less structured, with a canopy of approximately 1.0 m to 1.5 m tall due to a distinct dry season and scarce precipitation. (ii) Mangroves in the central Pacific have heights reaching up to 30 m as a result of an increase in precipitation and a shorter dry season. (iii) Mangroves in the South Pacific coast comprise the most complex mangrove systems with trees >40 m tall, which is partly due to optimal rainfall and high levels of freshwater supply throughout the year [8].
The Gulf of Nicoya is located between the north and central Pacific of Costa Rica (Figure 1a), spanning 1530 km2 between the Tempisque, Barranca, and Grande de Tárcoles rivers. These rivers create a highly productive mangrove ecosystem due to their large sediment and nutrient deposition [9]. Mangroves in the Gulf of Nicoya cover an area of 20,000 ha, and their growth is promoted by the balance between the river freshwater flowing into the gulf and the ocean water entering the gulf [10]. The main mangrove species of the Gulf include Rhizophora mangle, Rhizophora racemosa, Avicennia germinans, Avicennia bicolor, and Laguncularia racemosa followed by the less abundant Pelliciera rhizophorae [9,11,12]. Mangrove ecosystems in the Gulf of Nicoya have been widely studied [10], which is partly because of their relevant contributions to Costa Rica’s economy [13].
Ecological growth conditions affect the xylogenesis of trees [14]. This is particularly true in mangrove ecosystems due to the extremely different growth conditions compared to terrestrial forests [15]. Specifically, tides and salinity determine the anatomical features of the trees [16]. According to Quadros et al. [17], mangrove ecosystems have been included in tropical moist forests, which is probably based on the assumption that mangrove trees show similar traits and trade-offs to terrestrial tropical trees. However, the ecological components of mangroves can be expressed through different functional, terrestrial, or anatomical traits [18]. Their deeper investigation can explain the behavior of these ecosystems, the growth dynamics, and the developments of mangrove forests [18,19].
Ecological anatomy studies of mangroves have mainly focused on salinity and flood frequency [16]. Studies have shown that vessel elements under these conditions are slightly smaller than vessels produced during the rainy season [17]. Other studies [20,21,22,23,24,25] suggest that anatomical features of mangrove trees, mainly functional characters, tend to change with ecological conditions, implying that the variation in anatomical structure has a functional significance for the ecological adaptation of mangroves.
Furthermore, growth rings in mangrove trees can adapt to salinity conditions [18,26]. In contrast to Naskar and Palit [16], recent studies have demonstrated that certain growth conditions in mangrove ecosystems produce growth rings in some species [27]. Advanced techniques such as ionic radiation demonstrated the presence of a growth ring boundary that was not previously observed under light microscopy, and such growth rings were called “indicative” [28]. In tropical America, unlike other regions of the world, there is additional uncertainty regarding the formation of growth rings in mangrove trees, as some species exhibit growth rings while others do not. Namely, growth rings were reported in Rhizophora mangle and Laguncularia racemosa in Brazil [27,29,30,31] and Colombia [32].
Despite these advances, there is still a lack of research on the adaptation of anatomical structure and growth ring formation to ecological conditions for supporting mangrove growth in Central American mangroves. Thus, we used the methods and principles of ecological anatomy to explore the relationship between ecological factors and ring formation, anatomical characteristics, and other wood properties of six mangrove tree species. More specifically, we used three sites with differing environmental conditions in the Gulf of Nicoya in Costa Rica to elucidate the adaptive capacity of wood structures to different environmental conditions of this region.

2. Materials and Methods

2.1. Mangrove Species and Study Site

The following 6 species were studied: Avicennia bicolor Standl (Acanthaceae), Avicennia germinans L. (Acanthaceae), Laguncularia racemosa (L.) C.F. Gaertn (Combretaceae), Pelliciera rhizophorae Planch. & Triana (Tetrameristaceae), Rhizophora mangle L. (Rhizophoraceae) and Rhizophora racemosa G. Mey. (Rhizophoraceae). These mangrove species were chosen by their abundance and were grown naturally in the Gulf of Nicoya [9,11,12].
We chose three sites located in the central and north Pacific coast of Costa Rica, within the Gulf of Nicoya (Figure 1a), to represent a salinity gradient. Site 1 is near the town of Chomes (10°12′37.94″ N–85°13′00.64″ W), site 2 is within the Cipancí National Wildlife Refuge (RNVS) (10°02′00.73″ N–84°54′03.49″ W) and site 3 is located in Río Seco-Chacarita (10°00′01.46″ N–84°46′33.73″ W). Mangroves grow along the coastline of this site (Figure 1a) and are directly influenced by the tides and the exchange of salt and freshwater as well as the flux of sediments and flooding regime. Across sites, salinity (measured at 40 cm depth) was intermediate at 27.05 PSU (1 PSU equals 1 part per thousand-ppt) at site 1, highest at site 2 (38.6 PSU) and lowest at site 3 (18.95 PSU). The site conditions, climatic features, and other characteristics are detailed in Table 1.

2.2. Tree Samples

Three trees per species were sampled at every site (6 mangrove species × 3 sites × 3 tree samples = 54 trees). The diameter at breast height (DBH) was measured, but in individuals with aerial prop roots, the diameter was measured at 10 cm above the top root. Samples consisted of an increment core of 12 mm diameter and 50 mm long (Figure 1b) and were extracted using a 12 mm core bit (Figure 1c) and a battery-powered drill (Drill Dewalt 20V, Towson, MD, USA, Figure 1d,e). Two different samples were taken from each tree, one from the north side of the tree and the second from the south side of the tree. Samples were obtained 50 cm above the topmost root or at breast height (1.3 m above the ground) in trees without prop roots.

2.3. Physical Properties and Carbon Content Determination

First, the increment cores were registered in the Xylariorum of the Technological Institute of Costa Rica (TECw). Full samples were cut into three subsamples of 1 cm, 2 cm, and 3 cm lengths, and they were used for permanent anatomy slice, specify gravity determination, and annual growth presence, respectively. The 2 cm long subsample cores were weighed, and their diameter and length were measured with a precision of 0.01 for volume determination. After these samples were dried in an oven at 103 °C for 24 h, they were weighed again. The calculation of the green moisture content (MC) refers to the moisture content when the sample is extracted from the trunk, which is commonly referred to as green MC, according to the D-4442 standard [33]. The specific gravity (SG), the ratio of the density of wood to the density of water at 4.4 °C, and the commonly determined dry weight/green volume of volume of subsamples) was determined by the D-143 standard [34]. For determining green density (GD), the green weight/green volume ratio was used. Dry 2 cm long subsamples were milled and sieved through 0.25 mm and 0.42 mm meshes (#40 to #60 mesh, respectively) until approximately 6 g per test was obtained. The carbon fraction (C) was determined by means of organic elemental analysis, using the Vario EL CUBE model (Elementar, Langenselbold, Germany).

2.4. Wood Sample Preparation for Ring Boundary Identification

Subsamples were pasted with polyvinyl acetate (PVA) on a wood support with their cross-section upwards. Subsequently, thin cross-sections were sanded with 100, 200, 400, 800, and 1200 grit sandpaper. Then, the samples were observed for the annual ring boundary and its distinctiveness. This distinctiveness was associated with anatomical markers, which can be macroscopic or microscopic [35]. Despite different classification systems [36], that proposed by Worbes and Raschke [37] was used because of its higher dendrochronological orientation. The classification considers two elements: (i) distinctiveness is established in 3 categories: distinctive or boundary defined (+), indistinctive or boundary non-defined (−), and more or less distinctive (+/−), and (ii) type of annual ring, which is based on the structure of growth zones and the anatomical structure. According to Worbes [38], there are five established types of annual rings:
  • Density variation: The annual ring boundary is marked by several rows of fibers with fibers having a shortened radial diameter and thickened walls.
  • Marginal parenchyma: The annual ring boundary is marked with a uniseriate or multiseriate marginal parenchyma band.
  • Fiber/parenchyma pattern: The boundary is marked by periodically recurring patterns of alternating parenchyma and fiber bands.
  • Vessels distribution: There is a variation in the diameter or frequency of vessel elements.
  • Fiber band: The annual ring boundary is marked by a band of fibers.

2.5. Permanent Slide Preparation and Wood Anatomical Description

The 1 cm long subsample was softened in hot water for 1 h. Tangential, radial, and transverse sections of the subsample were cut (12–15 μm thick) and were stained with safranin and dehydrated with a series of alcohols (5 min each in 10%, 20%, 30%, 40%, 50%, 70%, and 95%). Finally, sections were rinsed and mounted on microscope slides. Furthermore, a small piece was cut from each wood block to prepare macerated wood using Franklin’s method [39]. The IAWA list [40] was used for choosing wood identification characteristics with some modifications to allow for increased accuracy and subsequent species-level separation. The quantitative anatomical features measured in wood were the length and diameter of the fibers, lumen diameter, cell wall thickness, vessel length, diameter and frequency of pores, solitary pore frequency, diameter of intervessel pits, and height and width of rays. Fiber dimensions and vessel lengths were measured on macerated wood. Permanent slides were used for the measurement of the other anatomical characters. Qualitative anatomical features were also determined using the IAWA List as a guide [40].

2.6. Statistical Analysis

Data measured, DBH, MC, GD, SG, C content, dimension of vessels (length and diameter), pores frequency, fiber dimensions (length, lumen diameter, fiber diameter, cell wall thick), ray dimensions (height, width) and ray frequency were analyzed for their normality and presence of outliers. After that, an analysis of variance using a General Lineal Model (GLM) was applied for each parameter to determine the species or site and their interaction effects. The Tukey test was used to test the mean difference at a p < 0.01. SAS 8.1 for Windows (SAS Institute Inc., Cary, NC, USA) was used to carry out the statistical analyses.

3. Results

3.1. Growth Rings

Avicenna bicolor and A. germinans growth rings were well defined by successive xylem rings alternating with the phloem (Figure 2(a-1,a-2,a-3,b-1,b-2)). Likewise, the anastomosing of successive cambia was evident in the two species at the three sites (white arrow in Figure 2(a-1,a-2,a-3,b-1,b-2)). At a microscopic level, the growth zone boundary was limited by a marginal band of parenchyma formed by more than three rows of parenchyma, and all parenchyma cells had prismatic crystals (Figure 3a). The rings that bifurcate for the growth-layer network (Figure 3c) exhibit an identical phenomenon, i.e., their width remains constant after they become defined (Figure 3b).
Laguncularia racemosa had a poorly defined growth zone boundary, a non-defined boundary or an indistinctive boundary; thus, the categories observed were null and type 3 with the boundary marked by periodically recurring patterns of alternating parenchyma and fiber bands (Figure 2). In addition, in L. racemosa trees from sites 1 and 2, the growth zone boundary was indistinctive (Figure 2(c-1)), but trees from site 3 presented more or less distinctive type 1 boundaries (+/−) (Figure 2(c-2,c-3)), which were marked by several rows of fibers with a shortened radial diameter and thickened walls (Figure 3f). The microscopic cross-section confirmed that in trees from site 1, the growth zone is well defined (Figure 3d); meanwhile, the growth zone of trees from sites 2 and 3 were indistinctive (Figure 3e).
In P. rhizophorae, the growth zone boundary was difficult to observe microscopically (Figure 3g–i). In contrast, the macroscopic observation was more effective and revealed that the growth zone boundary was poorly defined in samples from all three sites (Figure 2(d-1–d-3)). The growth zone was type 1 with density variation [38]. The growth zone of the two Rhizophora species was poorly defined in all three sites, and the boundary was marked by a band of fibers (Figure 2e,f), placing them in Worbes’ [38] Type 5 category. However, the microscopic cross-section showed contradictory results that were poorly defined in R. mangle from sites 1 and 2 and in R. racemosa from sites 2 and 3 (Figure 3i–k,n,o). Meanwhile, R. mangle in site 3 and R. racemosa site 1 showed a growth zone boundary marked by a band of fibers (Figure 3l–m).

3.2. Tree Diameter, Physical Properties, and Carbon Content

The tree diameter was different across the species, site, and species x site categories (Table 2). Both Avicennia species had the largest diameters, which were followed by R. racemosa, R. mangle, L. racemosa, and P. rhizophorae. Site 3 had the greatest diameter for A. bicolor, A. germinans, L. racemosa, R. mangle, and R. racemosa, whereas no statistical differences were found in these species at the other two sites. No statistical differences were found among the P. rhizophorae samples across sites (Table 3). Species effect on physical properties was only significant for green MC; the three effects (species, site, and species x site) were significant in GD and SG. Green MC was the highest in P. rhizophorae, which was followed by A. germinans, A. bicolor and L. racemosa, and the two Rhizophora species with the lowest values of MC.
No statistical differences in MC were found between sites for any of the six mangrove species. The values of GD and SG were the highest in the two species of Rhizophora, and significant differences between the two Avicennia species were observed. Although GD values were similar between L. racemosa and P. rhizophorae, SG values were significantly lower in P. rhizophorae compared to L. racemosa. The site effect was significant only in L. racemosa and R. racemosa with the lowest GD and SG found in site 3 (Table 3). Finally, the C content varied with species and site, but the interaction between species and site was not significant (Table 2). In relation to species, the lowest C content values were observed in A. bicolor in site 2, and the highest values were presented in L. racemosa in site 2 (Table 3).

3.3. Anatomical Description

3.3.1. General Vessel Description

We observed diffuse porosity in the six mangrove species and sites studied, but the vessel arrangement was different between species (Table 4). A radial pattern was observed in two Avicenna species (Figure 3a–c) and in the P. rhizophorae trees from site 3 (Figure 3i).
The vessel grouping in radial multiples of four or more cells was observed in P. rhizophorae trees across all sites (Figure 3g–i) and the R. racemosa trees of site 1 (Figure 3m). The frequency and dimensions (length and diameter) of vessels were different among species, site, and the interaction species x site (Table 2). The highest vessel frequency (20–37 pores/mm2) was found in Avicennia species, which was followed by P. rhizophorae and Rhizophora species, and the lowest frequency (6–10 pores/mm2) was observed in L. racemosa (Table 4). However, the length of the vessel presented contradictory results; the longest vessels were observed in Rhizophora species and in P. rhizophorae (between 435 and 588 µm), whereas the shortest vessel length (258–283 µm) was observed in A. bicolor. The largest vessel diameter was observed in L. racemosa (83 to 102 µm), which was followed by Rhizophora and Avicennia species, and the narrowest (56–60 µm) was seen in P. rhizophorae (Table 4). A simple perforation plate was observed in four species (two Avicennia species, L. racemosa and P. rhizophorae), and a scalariform perforation plate was observed in Rhizophora species (Figure 4a).
A reticulate perforation plate was observed in R. mangle trees from site 3 (Figure 4b) but not in R. racemosa. Five species (two Avicennia species, P. rhizophorae, and R. racemosa) presented alternate intervessel pits, while A. bicolor and A. racemosa presented scalariform pits (Figure 4c) and L. racemosa presented intervessel pits with alternating polygonal shapes and vestured (Figure 4e). Deposits in the lumina of vessels were observed only in gums in trees of L. racemosa from site 1 (Figure 4d), and neither tyloses nor gums were viewed in other species. Laguncularia racemosa did not present tyloses, which was probably due to samples being extracted from sapwood. Vessel-ray pitting was uniform and there were distinct borders, similar to intervessel pits in size and shape throughout the ray cell (Figure 4f,g). However, R. racemosa and R. mangle presented vessel-ray pits with reduced borders to apparently simple horizontal (gas-like) to vertical pits (Figure 4h), restricted to marginal rows.
According to IAWA class: 5: diffuse–porous, 7: vessels in diagonal and/or radial pattern, 10: vessels in radial multiples of 4 or more common; 11: vessels clusters common, 13: simples perforation plates; 15: Scalariform perforation plates with ≤10 bars, 19: reticulate perforation plate, 20: intervessel pits scalariform, 22: intervessel pits alternate, 23: shape of alternate pits polygonal, 30: vessel-ray pits with distinct borders; similar to intervessel pits in size and shape throughout the ray cell, 31: vessel-ray pits with significantly reduced borders to apparently simple: pits rounded or angular, 32: vessel-ray pits with significantly reduced borders to apparently simple: pits horizontal (scalariform, gash-like) to vertical, 34: vessel-ray pits unilaterally compound and coarse (over 10 µm), 35: vessel-ray pits restricted to marginal rows (IAWA, 1989). “−” anatomical feature absent, “+” anatomical feature present, “?” unknown feature. IVP = intervessel pit.
Vessel diameter: There were statistical differences in frequency and vessel dimensions (length and diameter) of vessels by sites and by species x site (Table 2). The anatomical feature exhibiting the maximum differences was vessel frequency: site 2 was statistically different from the other two. Vessel frequency was statistically different in all sites for P. rhizophorae, whereas site 3 presented the lowest frequency for A. germinans (Table 4). Trees from site 2 produced the highest vessel frequency in A. bicolor and L. racemosa, but the frequency was the lowest in R. mangle and R. racemosa. The vessel length was shortest in site 1 for A. bicolor and site 3 for R. mangle, but the longest diameter was found in site 1 for P. rhizophorae. Vessel diameter was different between species (p = 0.01), and by site (p = 0.05) (Table 2). A statistically significant difference in vessel diameter was observed in A. germinans, L. racemosa, and two species of Rhizophora species.
We found substantial differences in vessel grouping between P. rhizophorae and R. mangle. P. rhizophorae trees from site 3 had vessels in radial multiples of four or more (Figure 3i), while trees from sites 1 and 2 presented vessels in the radial orientation of two to four cells (Figure 3g,h). In addition, trees from site 2 also presented a higher frequency of vessels in multiples of four cells compared to trees from site 1 (Figure 3g,h and Figure 5a,b). Meanwhile, R. mangle trees from site 1 showed the presence of vessels in radial multiples of four, while trees of this same species growing in the other two sites (Figure 3m) did not present this anatomical feature (Figure 3n,o).
We found reticulate perforation plates in R. mangle trees at site 3 (Figure 4b) and scalariform perforation plates in trees from the other two sites (Figure 4a). The remaining five mangrove species had similar perforation plates among sites. Tyloses feature in the lumina of vessels of A. bicolor and L. racemosa, one of these was found in our study. Gums were present in R. racemosa trees at site 1 (Figure 4c) but absent elsewhere.
Vessel-ray pits were unilaterally compound and coarse (over 10 µm) in P. rhizophorae at site 1 (Figure 3f); meanwhile, at the other two sites, the trees presented vessel-ray pits with distinct borders like intervessel pits, varying in size and shape throughout the ray cell.

3.3.2. Fibers

Quantitative features (length and diameter of the fiber, lumen diameter, and wall cell thickness) were different among species and by interactions between species × site, except for fiber diameter, which was not significantly different across sites (Table 2). The longest fiber and widest diameter were observed in R. racemosa, followed by R. mangle, A. bicolor, and A. germinans, and the shortest fiber was measured in L. racemosa (Table 5). The lumen diameter was widest in P. rhizophorae, followed by L. racemosa and Avicennia sp., and it was narrowest in Rhizophora sp. The thickest cell wall was observed in Rhizophora species, followed by P. rhizophorae and L. racemosa, while the thinnest wall cell was observed in Avicennia species (Table 5).
There were no differences in qualitative anatomical features (fiber stored crystals, septate, ground tissue fiber, or fiber pits presence) and no presence of stored fibers and crystals across sites for any of the mangrove species (Table 5). Septate in fibers was observed in all trees of P. rhizophorae across sites (Figure 5a). Similarly, fiber pits, both radial and tangential, were common in R. mangle and R. racemosa across sites (Figure 5b,c). R. mangle presented ground tissue fiber (Figure 5d), which was not observed in R. racemosa. Helical thickening in the ground fiber was observed in R. mangle (Figure 5d) but not in R. racemosa.

3.3.3. Ray Parenchyma

Quantitative parameters (ray height, ray width cell, and ray frequency) differed statistically by species across sites but not across analysis categories and the interaction species x site (Table 2). Two species of Rhizophora had the tallest rays (from 750 to 948 µm), followed by P. rhizophorae, A. germinans, and A. bicolor, while the species with the shortest ray height (190 to 268 µm) was L. racemosa (Table 5). The widest ray was found in Rhizophora (from 90 to 115 µm), which was followed by Avicennia and P. rhizophorae. The species with the narrowest rays (14 to 21 µm) was L. racemosa (Table 5). The highest ray frequency was found in P. rhizophorae, with average values of 30 ray/mm2, followed by L. racemosa and Avicennia species. In contrast, the lowest ray frequency (6.8 to 8.7 ray/mm2) was observed in R. racemosa. We found significant differences across sites in all species and each ray dimension; ray height was statistically different in A. bicolor and L. racemosa, and site 2 was statically different from sites 1 and 3. Meanwhile, the ray width in all species was statistically different in all sites of L. racemosa, P. rhizophorae, and R. mangle. The ray width of the Avicennia species and R. racemosa in site 3 was statistically different than in sites 1 and 2 (Table 5). Ray frequency was similar across sites in Avicennia and P. rhizophorae but significantly different in L. racemosa in site 3 and R. mangle and R. racemosa in site 2.
Despite the differences in certain anatomical features between species, none of the species presented stored rays. Exclusively uniseriate rays were observed in L. racemosa and P. rhizophorae (Figure 6a,b), while Avicennia species presented 1–3 seriate rays (Figure 6c), and Rhizophoraceae species presented 3–6 seriate rays (Figure 6d). Rays with height >1 mm were observed in the Avicennia and Rhizophora species (Figure 6c,d). Disjunctive ray parenchymal cell walls were observed in site 1 of L. racemosa (Figure 6e), and the rays of P. rhizophorae and R. racemosa look like this anatomical feature (Figure 6f,g). The two Rhizophora species had all procumbent ray cells and upright and/or square cells (one to four rows). P. rhizophorae had all ray cells upright and/or square. Meanwhile, in A. bicolor and A. germinans, all rays were formed by upright and/or square cells or rays with procumbent body cells and upright and/or square cells (one to four rows). L. racemosa species presented a ray with procumbent, square, and upright cells mixed throughout the ray, and P. rhizophorae was observed to possess all procumbent ray cells. Crystals of different prismatic shapes located in procumbent, square, and upright cells were present in all species except in A. germinans, L. racemosa (Figure 6i–k) and P. rhizophorae. Raphide crystals were observed only in P. rhizophorae (Figure 6l).
We found many anatomical features of ray cells differed across sites in all mangrove species (Table 6). Ray cell height was not affected in Rhizophora species, but it was affected in species of Avicennia, L. racemosa, and P. rhizophorae (Table 5). The tallest and shortest ray cells were observed in site 2 for A. bicolor and L. racemosa, respectively. Ray width was different across all six species of mangroves (Table 5). However, ray cells of three species (A. bicolor, P. rhizophorae, and R. mangle) presented different quantity of cell seriate, affecting the ray width dimension. A. bicolor presented a ray width with 1–3 seriate in sites 1 and 2, but 1–5 seriate in site 3 (Figure 6c), the latter having the widest rays (Table 5). Similar traits were observed in P. rhizophorae, wherein the rays in trees from sites 1 and 2 were exclusively solitary (Figure 6a). Meanwhile, rays were 1–3 seriate in trees from site 3 (Figure 6b), producing rays with wider dimensions (Table 5). In R. mangle, the number of cells in ray width was similar in trees from sites 1 and 2 (1–3 seriates), but the rays were composed of 4–10 seriates in site 1 trees (Figure 6d), producing wider rays. The ray width was 1–3 seriate in A. germinans in all sites, but it was the narrowest in site 3 (Table 6). The same tendency was found in the ray width of L. racemosa and R. racemosa, wherein the quantity of cells in ray width was similar but the dimensions in width were statistically different across the three sites (Table 5).
We found site effects in cell compositions in two species of Avicennia, L. germinans, P. rhizophorae and two species of Rhizophora (Table 5). P. rhizophorae trees in site 3 had procumbent, square, and upright cells mixed throughout the ray (Figure 7a), with differences in trees of sites 1 and 2, which presented all ray cells with upright and/or square cells (Figure 7b). R. mangle and R. racemose from sites 1 and 3, respectively, presented procumbent body ray cells with mostly two to four rows of upright and/or square marginal cells (Figure 7c), but all ray cells across sites were procumbent or body ray cells were procumbent with one row of upright and/or square marginal cells. The presence of crystals seemed independent of site: A. germinans, L. racemosa, and P. rhizophorae did not possess any crystals (Figure 6h,i) in sites 1 and 3, respectively. Raphide crystals were observed in P. rhizophorae at two sites (Figure 6l). Finally, L. racemosa presented disjunctive ray parenchymal cell walls in two sites and P. rhizophorae, and R. racemosa in one site (Figure 6f,g).

3.3.4. Ray Parenchyma

Five mangrove species (A. bicolor, A. germinans, P. rhizophorae and two Rhizophora species) presented limited apotracheal and paratracheal parenchyma (Figure 3a–f, Table 6), while L. racemosa presented visible and abundant paratracheal parenchyma (Figure 3d–f). Banded parenchyma was only present in the two Avicennia species (Figure 3a–c). The lack of visibility of the axial parenchyma in P. racemosa and two Rhizophora species made it difficult to determine the quantity of cell/strand length of axial parenchyma (Figure 8i). The crystalline presence of axial parenchyma was observed only in two Avicennia species. In addition, these two species presented concentric phloem (Figure 8c, Table 6). None of the mangrove species presented stored axial parenchyma.
We found stable axial parenchyma with few differences across sites (Table 6). Apotracheal parenchyma was not observed in A. bicolor at site 1, but it was observed in the other two sites (Figure 8a). Axial parenchyma unilateral paratracheal with over eight cells per parenchymal strand (Figure 8f) and more than one crystal of about the same size per cell were observed in sites 1 and 2. In A. germinans, axial parenchyma and unilateral paratracheal were absent in site 2 but present in the other two sites (Figure 8c). L. racemosa presented apotracheal parenchyma, vasicentric parenchyma, and axial parenchyma unilateral paratracheal in site 1 (Figure 8d), while sites 2 and 3 presented axial lozenge-aliform and confluent parenchyma (Figure 8e). The cell composition also varied between sites; 5–8 cells per parenchyma strand were observed in L. racemosa (Figure 8g), while (Table 6) P. rhizophorae trees presented apo tracheal and scanty paratracheal parenchyma and 3–4 cells per parenchymal strand in all sites (Figure 8h). Trees from site 1 had 2 cells per parenchymal strand, but this anatomical feature was not observed in the other two sites. For the two species of Rhizophora, axial parenchyma and cell composition were difficult to differentiate. Apotracheal parenchyma was observed in R. racemosa in site 2 (Figure 8b) and the cell composition in R. mangle in site 2 (Figure 8i).

4. Discussion

4.1. Growth Rings

We found limited growth ring boundaries for all mangrove species at the macroscopic (Figure 2) and microscopic level (Figure 3). However, in Avicennia, the growth zone boundary was well defined across our sites by successive xylem rings alternating with phloem (Figure 2a,b) with occasional bifurcate annual rings also visible. Our findings match those of Nazim et al. [41] and Schmitz et al. [22,42], who report that under limited growing conditions, these growth zone rings are annual in nature. In addition, the bifurcate and growth-layer networks in Avicennia (Figure 3c) were similar across sites (Table 2), which is common in this species [22,41,42]. Despite all this, the formation of a growth zone including phloem may be the result of the endogenous control of cambium activity, which does not indicate the age of the tree [43]. Another important result was that the growth ring was similar in the three sites studied, suggesting that the ecological condition did not affect the growth rings in this species. Hence, although the growth rings of two species of Avicennia were observed and cataloged with a high intensity of expression, our finding should be taken with caution, because despite there being some contradictory reports in the literature, there is agreement that Avicennia species lack annual growth rings [44].
Rhizophora species are distributed widely across the tropical coasts of the world [45] (Ellison, 1991); thus, this genus garners considerable attention in relation to growth ring formation [27,29,32,46,47]. In general, the formation of growth zones is related to climatic seasonality; the distinctiveness of growth rings improves when seasonality is well defined [27]. Likewise, sites with high salinity help define growth ring boundaries [27,29,32]. We found limited growth ring boundaries in all our sites (Figure 2e,f and Figure 3j–o), although a well-defined seasonality is present (Table 1). Another important difference between our study and previous reports is that the growth zone boundary was marked by a band of fibers and not by the difference in diameter and frequency of vessels as observed by Souza et al. [27], Verheyden et al. [21,46], Schmitz et al. [47] and Ramírez Correa et al. [32]. Thus, we hypothesize that variations in salinity and freshwater inputs over time may be producing the poor definition of the growth zone in Rhizophora specie, as observed in site 1 for R. racemosa and site 3 in R. mangle (Figure 2a,b). We cannot confidently infer the influence of other environmental variables not studied in the present study. Longer-term monitoring of salinity, freshwater inputs and other variables known to be relevant to mangrove growth are necessary to arrive at a more robust conclusion.
To our knowledge, this study is the first to report the presence of annual rings in L. racemosa, which precludes us from generalizing the lack of distinctiveness of the growth zone beyond the coasts of Costa Rica. In addition, our findings contradict those from Estrada et al. [30], who reported macroscopically well-defined growth rings with alternating light brown and dark brown layers in L. racemosa. In contrast, we found growth rings were limited by periodically recurring patterns of alternating parenchyma and fiber bands (Figure 2).
The ecological conditions affected growth ring formation. Sites 2 and 3 with similar growing conditions produced similar growth rings, but the growing conditions at site 1 are different from those of sites 2 and 3 (Figure 3e,f), which is probably due to the influence of freshwater, different salinity and direct tidal effects, which produced well-defined growth rings (Figure 3d). The L. racemosa trees at site 1 did not show any type of ring marking unlike the trees in sites 2 and 3. This is possibly due to the ecological conditions of site 1, specifically the influence of freshwater from nearby rivers and streams and the direct influence of tides and winds in this site that are not present in the other sites, which produce conditions that render it less likely to produce anatomical markers to evidence the growth ring boundary.
This study presented a detailed observation of the growth rings in these six types of mangroves in Costa Rica, and we found that ecological conditions affected different species differently. A. bicolor, A. germinans, P. rhizophorae and two species of Rhizophora were affected by ecological conditions, but L. racemosa was not affected by ecological conditions.
A. bicolor, A. germinans, L. racemosa, R. mangle, and R. racemosa may be suitable for use in dendrochronological studies focusing on ecological, climatic, morphological, and other research criteria alongside the Costa Rican coast. However, additional studies on tree markings, dendrometers, and dating, among other techniques, should be carried out to help confirm the frequency and boundary of growth rings in mangrove trees and the factors that influence this formation. Positive results could improve the applicability of the formation of growth rings in future research that contributes to the understanding of the climate and ecology of mangrove ecosystems.

4.2. Wood Anatomy

The most significant anatomical features related to ecological growth conditions are the size and arrangement of vessels, the size and frequency of rays, fiber dimensions, and the presence of special anatomical features such as tracheids, pits, and perforation plates [48].
We found vessels and rays were the most affected by site conditions. For example, we observed that wood from P. rhizophorae (Figure 3i) and two Avicenna species (Figure 3a–c) had different vessel grouping, rays dimensions, and composition in site 3 compared to wood from the other two sites.
The other anatomical features or other properties evaluated also differed by the site or the species (Figure 9). For instance, physical characteristics like green density, SG, and carbon content were only statistically significant across sites (Figure 9a). The lack of difference in physical properties was probably influenced by the diameter of the sampled tree [49], which was probably due to our sample being extracted from the external part of the trunk for assessing physical properties. DBH ranged broadly among species and sites (Table 2); trees of Avicennia, Rhizophora spp. and P. rhizophorae had larger DBH values at site 3 than the trees at sites 1 and 2, while the opposite was true for L. racemosa trees (Table 3).
Although mangrove ecosystems are affected by many factors [2], the difference in the diameter of trees can be influenced by freshwater [50]. Freshwater inputs are essential to maintain the stability of salinity gradients, circulation patterns, water quality, influx of organic carbon, nutrients and sediment, flushing of the ecosystems, distribution and abundance of many species. However, excessive freshwater inflow and flooding can result in low-salinity stress to flora, increased sedimentation, density stratification, oxygen depletion, and nutrient and contaminant transfer [51]. These dynamics are present in sites 2 and 3, which were more strongly influenced by freshwater, but absent in site 1, thus confirming our hypothesis.
We also found that species was the most important factor explaining the variations in wood anatomy (Table 2). The species with the most anatomy variation was L. racemosa, followed by P. rhizophorae (Figure 9b), while a similar variation was observed in Avicennia and Rhizophora species (Figure 9b), with the least variation observed in R. racemosa (Figure 9b). This sequence of species represents the most and least stable species in terms of variation in the anatomical and site condition of mangrove systems.
Site environmental conditions affect anatomical features of mangrove tree species, both in quantifiable parameters and categorical features (Figure 9a). We found that vessel frequency was the most affected (with 8 times varied the anatomy, Figure 9a), which was followed by the vessel diameter and vessel length, perforated plate, porosity, vessel pitting, and deposits presented limited wood anatomy variation (Figure 9a).
Salinity is a strong determining factor for the regulation of water transport in mangrove trees [52,53]. Verheyden et al. [21], for example, showed that vessel frequency in mangrove trees could be a potential indicator of past changes in water salinity. A high salt content reduces the availability of water in the plants, leading to a phenomenon known as a physiological drought [52]. Therefore, safe transport conditions must be developed to balance cavitation and efficient hydraulic conductivity [31]. In essence, the plant modifies the size and frequency of the vessels to minimize these salinity effects [31,43,47]. Therefore, the variation in the salinity conditions at the three study sites could explain the variation in porosity, grouping, frequency, and fewer effects on vessel sizes between sites. This result agrees with studies carried out by Schmitz et al. [47], Yañez et al. [54], and Robert et al. [24], who suggest that the diameter and width dimensions of vessels were less affected by salinity conditions.
Interestingly, we observed that the radial multiple grouping varied among sites (Figure 9a). Also, a radial vessel pattern was observed in two Avicenna species (Figure 3a–c) and P. rhizophorae trees from site 3 (Figure 3i) and R. racemosa from site 1 (Figure 3m). The presence of vessel groups (in clusters or in a radial direction) is a plant strategy to prevent conductive systems blockage; clusters and radial grouping is an alternate conduit whereby water can be carried in the same pathways if one or several vessels in a group are incapacitated or in case the plant is subjected to stress, mainly drought [55,56,57]. These same authors hypothesize that radial and cluster groups minimize the distance between two vessels, thus eliminating the possibility that embolized vessels would break the vessel group in two halves, disconnected by the air embolism. In addition to the multiple radials having a sequential arrangement, the conductive pathway represented by the innermost vessel in the series can be maintained if disabling proceeds centrifugally in a stem, as it has generally been observed.
Thus, the radial pattern observed in two species of Avicenna (Figure 3a–c) and P. rhizophorae trees from site 3 (Figure 3i) suggests that these species can be present under and adapted to unfavorable conditions. This hypothesis matches the ecological conditions of site 1, specifically, the influx of freshwater and probably the wind and tidal influence at this site that are not present in the other sites. This would impose poor growth conditions for the species, consequently producing different vessel arrangements or the presence of a reticulate perforated plate, which ensures an adequate conduction of liquids [58,59]. However, the radial pattern mentioned before was also observed in R. racemosa at site 1 (Figure 3m), which seems to suggest that this might be a species-dependent feature further controlled by site conditions.
Fiber dimensions were also affected by environmental site conditions (Table 2) but not by species (Table 5). An increase in cell wall dimensions and diameters is related to water conduction. These changes occur as a safety strategy to mitigate highly negative pressure conditions within the secondary xylem, to provide support to the vessels, and to prevent collapse and cavitation [31]. Rhizophora species and A. bicolor trees had similar fiber characteristics among sites; meanwhile, other species presented differences in cell wall diameter in some sites (Table 5). There are a few differences present in the fiber dimensions, which are anatomical features affected mildly by the environmental conditions of the growth site [60].
Specialized structures, such as the presence of septate in P. rhizophorae, and ground tissue fiber and fiber pits common in both radial and tangential R. mangle, are intrinsic to each species for performing specific functions, such as storing starch in case of septums [60]. The presence of ground tissue fiber and fiber pits helps liquids transit in adverse conditions [61,62]. No difference was observed among sites (Table 5); thus, we conclude that these structures are not anatomical indicators of differences in environmental conditions in mangrove systems.
Furthermore, the radial conduction system (ray parenchyma) of trees was the most variable anatomical feature especially in the dimensions and composition of rays. For example, the number of ray width cells was the most affected anatomical feature (12 anatomy variations) followed by ray height with eight anatomy variations in the rays’ frequency (Figure 9). Ray cells are functional elements in wood structures that are responsible for the safe conduction of water under high negative pressure and are adaptive to intertidal ecological conditions [63]. Jantsh et al. [31] found that the widest rays are associated with soil with greater water restrictions and that ray width is fundamental in mangrove trees growing in areas with a constant physiological sequence. In addition, Zheng and Martínez-Cabrera [64] concluded that wide rays are related to conductivity, while narrow rays are more related to mechanical resistance. In our study, the width and height of the ray were the most variable anatomical features of all the structures studied (Figure 9a), suggesting that the different ecological conditions in the Gulf of Nicoya produce adaptive changes in wood ray anatomy in the mangrove species. Despite the observed variation, there was no clarity regarding the effects of environmental conditions in ray dimensions; in some species, there was a greater width in site 1, for example in A. bicolor, but in other species, site 3 presented the greatest variation, suggesting that the variations in dimensions were related to the site x species interaction (Table 2). This interaction effect will require further investigation.
Axial parenchyma differed to a lesser extent among sites (Figure 9a), thus highlighting their lower plasticity to adapt to the different environmental conditions of the mangrove ecosystems in the Gulf of Nicoya. Axial parenchyma performs multiple functions like storage and maintaining the condition of the vessels and is the less studied anatomical feature [65] despite the complex association between functions and vessels [66]. This probably explains why species in this study do not reflect important changes in anatomical structure (Figure 2) due to the ecological conditions of growth. This will also require further investigation.
The plasticity in ray (increasing of ray dimension) and vessel elements (multiple vessels) facilitates efficient hydraulic conductivity amidst negative growth conditions and physiological restrictions for mangrove trees, as presented in site 1, but this was not seen in sites 2 and 3. However, these conditions affected different mangroves species in in different way; for example, L. racemosa was the species with the highest changes.

5. Conclusions

We found that site 1 produced the highest quantities of changes in wood anatomy in mangrove tree species, with 38 changes in the wood structures, while sites 2 and 3 presented identical and fewer changes. Because the growing conditions at site 1 are different from those of sites 2 and 3, probably due to the influence of freshwater, different salinity and direct tidal effects in site 1, which affected anatomy of trees. These variations of ecological conditions were reflected in the growth ring formation of A. bicolor, A. germinans, P. rhizophorae and two species of Rhizophora but not L. racemosa.
Ray dimensions (height and width) are functional elements with a greater adaptability to site conditions. This plasticity allows mangroves in Nicoya Gulf to ensure water conductivity amidst negative growth conditions and physiological restrictions for trees. The grouping and arrangement of vessels also showed important anatomical variation, as expected in most mangrove trees, meaning that this type of structure must ensure efficient hydraulic conductivity.
L. racemosa was the species that presented the highest number of changes in anatomical characteristics across the different sites, which was followed by P. rhizophorae with a similar number of changes for Avicennia spp. and Rhizophora. We can thus conclude that the variations in the quantitative wood anatomical characteristics in L. racemosa, growing at different sites, are adaptations to fluctuating environmental conditions in the intertidal areas.

Author Contributions

Conceptualization, R.M., C.T. and D.T.-G.; methodology, R.M., C.T. and D.T.-G.; validation, R.M. and M.C.-J.; formal analysis, C.T.; investigation, R.M. and D.T.-G.; data curation, M.C.-J.; writing—original draft preparation, R.M. and C.T.; writing—review and editing, R.M. and D.T.-G.; supervision, M.C.-J.; project administration, D.T.-G.; funding acquisition, M.C.-J. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

All data are presented in this article and no data can be deposited.

Acknowledgments

The authors wish to thank the Vicerrectoria de Investigación y Extensión of the Instituto Tecnológico de Costa Rica (ITCR) for the economic support given to this research. This project was made possible by Conservation International through a donation from the Tierra Pura Foundation.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Maurya, K.; Mahajan, S.; Chaube, N. Remote sensing techniques: Mapping and monitoring of mangrove ecosystem—A review. Complex Intell. Syst. 2021, 7, 2797–2818. [Google Scholar] [CrossRef]
  2. Bimrah, K.; Dasgupta, R.; Hashimoto, S.; Saizen, I.; Dhyani, S. Ecosystem services of mangroves: A systematic review and synthesis of contemporary scientific literature. Sustainability 2022, 14, 12051. [Google Scholar] [CrossRef]
  3. Asari, N.; Suratman, M.N.; Mohd Ayob, N.A.; Abdul Hamid, N.H. Mangrove as a Natural Barrier to Environmental Risks and Coastal Protection. In Mangroves: Ecology, Biodiversity and Management; Rastogi, R.P., Phulwaria, M., Gupta, D.K., Eds.; Springer: Singapore, 2021. [Google Scholar] [CrossRef]
  4. Monika Yadav, A. A. A Holistic Study on Impact of Anthropogenic Activities over the Mangrove Ecosystem and Their Conservation Strategies. In Coastal Ecosystems; Madhav, S., Nazneen, S., Singh, P., Eds.; Coastal Research Library; Springer: Cham, Switzerland, 2022; Volume 38. [Google Scholar] [CrossRef]
  5. Alongi, D.M. Global significance of mangrove blue carbon in climate change mitigation. Sci 2020, 2, 67. [Google Scholar] [CrossRef]
  6. SINAC (Sistema Nacional de Áreas de Conservación). Costa Rica: Mapa de Ecosistemas de Manglar 2021. 2021 Programa Nacional de Humedales (SINAC)/Centro Agronómico Tropical de Investigación y Enseñanza (CATIE)/Conservación Internacional Costa Rica. Available online: https://storymaps.arcgis.com/stories/2dda39902299463085723bb35ace3c32 (accessed on 15 March 2024).
  7. Yaney-Keller, A.; Santidrián Tomillo, P.; Marshall, J.M.; Paladino, F.V. Using Unmanned Aerial Systems (UAS) to assay mangrove estuaries on the Pacific coast of Costa Rica. PLoS ONE 2019, 14, e0217310. [Google Scholar] [CrossRef]
  8. Silva-Benavides, A.M. Mangroves. In Marine Biodiversity of Costa Rica, Central America; Wehrtmann, I.S., Cortés, J., Eds.; Monographiae Biologicae; Springer: Dordrecht, The Netherlands, 2009; Volume 86. [Google Scholar] [CrossRef]
  9. Vargas, J.A. The Gulf of Nicoya: Estuarine ecosystem. In Costa Rican Ecosystems; Kappelle, M., Ed.; The University of Chicago Press: Chicago, IL, USA, 2016; pp. 139–161. Available online: https://books.google.co.cr/books?hl=es&lr=&id=My-7CwAAQBAJ&oi=fnd&pg=PA139&ots=i0j2SHttqG&sig=QphzNvLVLrnDRwctPVJ7KdJnI6M&redir_esc=y#v=onepage&q&f=false (accessed on 23 April 2024).
  10. Alms, V.; Wolff, M. Identification of Drivers of Change of the Gulf of Nicoya Ecosystem (Costa Rica). Front. Mar. Sci. 2020, 7, 707. [Google Scholar] [CrossRef]
  11. Zamora-Trejos, P.; Cortés, J. Los manglares de Costa Rica: El Pacífico Norte. Biol. Trop. 2009, 57, 473–488. [Google Scholar] [CrossRef]
  12. Carvajal-Oses, M.; Pérez-Molina, J.P.; Herrera-Ulloa, Á.; Moreira-Segura, C. Structure and composition of a mangrove forest on the Central Pacific coast of Costa Rica: Population of mollusks of commercial interest. Uniciencia 2024, 38, 98–116. [Google Scholar] [CrossRef]
  13. Hernández-Blanco, M.; Costanza, R.; Cifuentes-Jara, M. Economic valuation of the ecosystem services provided by the mangroves of the Gulf of Nicoya using a hybrid methodology. Ecosyst. Serv. 2021, 49, 101258. [Google Scholar] [CrossRef]
  14. Olson, M.E. From Carlquist’s ecological wood anatomy to Carlquist’s Law: Why comparative anatomy is crucial for functional xylem biology. Am. J. Bot. 2020, 107, 1328–1341. [Google Scholar] [CrossRef]
  15. Biswas, P.L.; Biswas, S.R. Mangrove Forests: Ecology, Management, and Threats. In Life on Land. Encyclopedia of the UN Sustainable Development Goals; Leal Filho, W., Azul, A.M., Brandli, L., Lange Salvia, A., Wall, T., Eds.; Springer: Cham, Switzerland, 2021. [Google Scholar] [CrossRef]
  16. Naskar, S.; Palit, P.K. Anatomical and physiological adaptations of mangroves. Wetl. Ecol. Manag. 2015, 23, 357–370. [Google Scholar] [CrossRef]
  17. Quadros, A.F.; Helfer, V.; Nordhaus, I.; Reuter, H.; Zimmer, M. Functional traits of terrestrial plants in the intertidal: A review on mangrove trees. Biol. Bull. 2021, 241, 123–139. [Google Scholar] [CrossRef] [PubMed]
  18. Hamalton, T.; Sahana, K.S. An overview of the adaptive variations in mangroves. Int. J. Agric. Environ. Biotechnol. 2022, 15, 851–860. [Google Scholar] [CrossRef]
  19. Wright, I.J.; Ackerly, D.D.; Bongers, F.; Harms, K.E.; Ibarra-Manriquez, G.; Martinez-Ramos, M.; Mazer, S.J.; Muller-Landau, H.C.; Paz, H.; Pitman, N.C.A.; et al. Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests. Ann. Bot. 2007, 99, 1003–1015. [Google Scholar] [CrossRef]
  20. Sun, Q.; Lin, P. Wood structure of Aegiceras corniculatum and its ecological adaptations to salinities. In Asia-Pacific Conference on Science and Management of Coastal Environment. Developments in Hydrobiology; Wong, Y.S., Tam, N.F.Y., Eds.; Springer: Dordrecht, The Netherland, 1997; Volume 123. [Google Scholar] [CrossRef]
  21. Verheyden, A.; De Ridder, F.; Schmitz, N.; Beeckman, H.; Koedam, N. High-resolution time series of vessel density in Kenyan mangrove trees reveal a link with climate. New Phytol. 2005, 167, 425–435. [Google Scholar] [CrossRef] [PubMed]
  22. Schmitz, N.; Verheyden, A.; Kairo, J.G.; Beeckman, H.; Koedam, N. Successive cambia development in Avicennia marina (Forssk.) Vierh. is not climatically driven in the seasonal climate at Gazi Bay, Kenya. Dendrochronologia 2007, 25, 87–96. [Google Scholar] [CrossRef]
  23. Ewers, F.W.; Lopez-Portillo, J.; Angeles, G.; Fisher, J.B. Hydraulic conductivity and embolism in the mangrove tree Laguncularia racemosa. Tree Physiol. 2004, 24, 1057–1062. [Google Scholar] [CrossRef] [PubMed]
  24. Robert, E.M.; Koedam, N.; Beeckman, H.; Schmitz, N. A safe hydraulic architecture as wood anatomical explanation for the difference in distribution of the mangroves Avicennia and Rhizophora. Funct. Ecol. 2009, 23, 649–657. [Google Scholar] [CrossRef]
  25. Jiang, X.; Choat, B.; Zhang, Y.J.; Guan, X.Y.; Shi, W.; Cao, K.F. Variation in xylem hydraulic structure and function of two mangrove species across a latitudinal gradient in Eastern Australia. Water 2021, 13, 850. [Google Scholar] [CrossRef]
  26. Sánchez, A.R.; Pineda, J.E.M.; Casas, X.M.; Calderón, J.H.M. Influence of edaphic salinity on leaf morphoanatomical functional traits on juvenile and adult trees of red mangrove (Rhizophora mangle): Implications with relation to climate change. Forests 2021, 12, 1586. [Google Scholar] [CrossRef]
  27. Souza, B.T.; Estrada, G.C.; Soares, M.L.; Callado, C.H. Occurrence of annual growth rings in Rhizophora mangle in a region with low climate seasonality. An. Acad. Bras. Ciênc. 2016, 88, 517–525. [Google Scholar] [CrossRef]
  28. Alves, E.E.N.; Rodriguez, D.R.O.; de Azevedo, P.; Vergütz, L.; Junior, L.S.; Hesterberg, D.; Ruiz, L.C.; Tomazello-Filho, M.; da Costa, L.M. Synchrotron-based X-ray microscopy for assessing elements distribution and speciation in mangrove tree-rings. Results Chem. 2021, 3, 100121. [Google Scholar] [CrossRef]
  29. Menezes, M.; Berger, U.; Worbes, M. Annual growth rings and long-term growth patterns of mangrove trees from the Bragança peninsula, North Brazil. Wetl. Ecol. Manag. 2003, 11, 233–242. [Google Scholar] [CrossRef]
  30. Estrada, C.D.; Callado, C.H.; Soares, L.G.; Lisi, S.L. Annual growth rings in the mangrove Laguncularia racemosa (Combretaceae). Trees 2008, 22, 663–670. [Google Scholar] [CrossRef]
  31. Jantsch, A.; Melo Júnior, J.C.F.D.; Amorim, M.W.; Larcher, L.; Soffiatti, P. Wood anatomy of Laguncularia racemosa (Combretaceae) in mangrove and transitional forest, Southern Brazil. Biol. Trop. 2018, 66, 647–657. [Google Scholar] [CrossRef]
  32. Ramírez Correa, J.A.; Molina Grajales, E.C.; Bernal Escobar, M. Anillos anuales y clima en Rhizophora mangle L. de la Bahía de Cispatá, Colombia. Rev. Fac. Nac. Agron. Medellín 2010, 63, 5639–5650. [Google Scholar]
  33. ASTM D4442-20; Standard Test Methods for Direct Moisture Content Measurement of Wood and Wood-Based Materials. ASTM International: West Conshohocken, PA, USA, 2020. [CrossRef]
  34. ASTM D143-22; Standard Test Methods for Small Clear Specimens of Timber. ASTM International: West Conshohocken, PA, USA, 2020. [CrossRef]
  35. Silva, M.; Funch, L.S.; da Silva, L.B. The growth ring concept: Seeking a broader and unambiguous approach covering tropical species. Biol. Rev. 2019, 94, 1161–1178. [Google Scholar] [CrossRef]
  36. Nath, C.D.; Munoz, F.; Pélissier, R.; Burslem, D.F.; Muthusankar, G. Growth rings in tropical trees: Role of functional traits, environment, and phylogeny. Trees 2016, 30, 2153–2175. [Google Scholar] [CrossRef]
  37. Worbes, M.; Raschke, N. Carbon allocation in a Costa Rican dry forest derived from tree ring analysis. Dendrochronologia 2012, 30, 231–238. [Google Scholar] [CrossRef]
  38. Worbes, M. Growth rings increment and age of trees in inundation forests, savannas and a mountain forest in the Neotropics. IAWA J. 1989, 10, 109–122. [Google Scholar] [CrossRef]
  39. Ruzin, S.E. Plant Microtechnique and Microscopy; Oxford University Press: New York, NY, USA, 1999; 322p. [Google Scholar]
  40. Wheeler, E.A.; Baas, P.; Gasson, P.E. IAWA list of microscopic features for hardwood identification. IAWA Bull. 1989, 10, 226–332. [Google Scholar]
  41. Nazim, K.; Ahmed, M.; Shaukat, S.S.; Khan, M.U.; Ali, Q.M. Age and growth rate estimation of grey mangrove Avicennia marina (Forsk.) Vierh from Pakistan. Pak. J. Bot. 2013, 45, 535–542. [Google Scholar]
  42. Schmitz, N.; Robert, E.M.; Verheyden, A.; Kairo, J.G.; Beeckman, H.; Koedam, N. A patchy growth via successive and simultaneous cambia: Key to success of the most widespread mangrove species Avicennia marina. Ann. Bot. 2008, 101, 49–58. [Google Scholar] [CrossRef] [PubMed]
  43. Robert, E.M.; Schmitz, N.; Boeren, I.; Driessens, T.; Herremans, K.; De Mey, J.; Hans Beeckman, H.; Koedam, N. Successive cambia: A developmental oddity or an adaptive structure? PLoS ONE 2011, 6, e16558. [Google Scholar] [CrossRef] [PubMed]
  44. Tomlinson, P.B. The Botany of Mangroves; Cambridge University Press: Cambridge, UK, 2016; 413p, ISBN 0-521-25567-8. [Google Scholar] [CrossRef]
  45. Ellison, J.C. The pacific palaeogeography of Rhizophora mangle L. (Rhizophoraceae). Bot. J. Linn. Soc. 1991, 105, 271–284. [Google Scholar] [CrossRef]
  46. Verheyden, A.; Kairo, J.G.; Beeckman, H.; Koedam, N. Growth rings, growth ring formation and age determination in the mangrove Rhizophora mucronata. Ann. Bot. 2004, 94, 59–66. [Google Scholar] [CrossRef]
  47. Schmitz, N.; Verheyden, A.; Beeckman, H.; Kairo, J.G.; Koedam, N. Influence of a salinity gradient on the vessel characters of the mangrove species Rhizophora mucronata. Ann. Bot. 2006, 98, 1321–1330. [Google Scholar] [CrossRef]
  48. Baas, P. Systematic, phylogenetic, and ecological wood anatomy—History and perspectives. In New Perspectives in Wood Anatomy; Baas, P., Ed.; Forestry Sciences; Springer: Dordrecht, The Netherland, 1982; Volume 1. [Google Scholar] [CrossRef]
  49. Santini, N.S.; Schmitz, N.; Lovelock, C.E. Variation in wood density and anatomy in a widespread mangrove species. Trees 2012, 26, 1555–1563. [Google Scholar] [CrossRef]
  50. Ellison, J.C. Factors Influencing Mangrove Ecosystems. In Mangroves: Ecology, Biodiversity and Management; Rastogi, R.P., Phulwaria, M., Gupta, D.K., Eds.; Springer: Singapore, 2021. [Google Scholar] [CrossRef]
  51. Mohammed, A.; Farrell, A.; Gobin, J.; Agard, J. Effects of Freshwater Flooding on Mangroves in the Caribbean Region; Department of Life Science, The University of the West Indies: St Augustine, Trinidad, 2014; Chapter 5; pp. 84–89. [Google Scholar]
  52. Kanai, H.; Tajima, M.; Sakai, A. Effects of salinity on the growth and survival of the seedlings of mangrove, Rhizophora stylosa. Int. J. Plant Soil Sci. 2014, 3, 879–893. [Google Scholar] [CrossRef]
  53. Parida, A.K.; Jha, B. Salt tolerance mechanisms in mangroves: A review. Trees 2010, 24, 199–217. [Google Scholar] [CrossRef]
  54. Yáñez-Espinosa, L.; Terrazas, T.; López-Mata, L.; Valdez-Hernández, J.I. Wood variation in Laguncularia racemosa and its effect on fibre quality. Wood Sci. Technol. 2004, 38, 217–226. [Google Scholar] [CrossRef]
  55. Carlquist, S. Vessel grouping in dicotyledon wood. Aliso 1984, 10, 505–525. [Google Scholar] [CrossRef]
  56. Carlquist, S. Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. Am. J. Bot. 1992, 79, 660–672. [Google Scholar] [CrossRef]
  57. Carlquist, S. Non-random vessel distribution in woods: Patterns, modes, diversity, correlations. Aliso 2009, 27, 39–58. [Google Scholar] [CrossRef]
  58. Meylan, B.A.; Butterfield, B.G. Occurrence of simple, multiple, and combination perforation plates in the vessels of New Zealand woods. N. Z. J. Bot. 1975, 13, 1–18. [Google Scholar] [CrossRef]
  59. Oskolski, A.A.; Jansen, S. Distribution of scalariform and simple perforation plates within the vessel network in secondary xylem of Araliaceae and its implications for wood evolution. Plant Syst. Evol. 2009, 278, 43–51. [Google Scholar] [CrossRef]
  60. Plavcová, L.; Olson, M.E.; Jandová, V.; Doležal, J. Parenchyma is not the sole site of storage: Storage in living fibres. IAWA J. 2023, 44, 465–476. [Google Scholar] [CrossRef]
  61. Pratt, R.B.; Castro, V.; Jacobsen, A.L. The functional significance of tracheids co-occurring with vessels in xylem of Eudicots suggests a role in embolism tolerance. IAWA J. 2023, 44, 477–494. [Google Scholar] [CrossRef]
  62. Echeverría, A.; Petrone-Mendoza, E.; Segovia-Rivas, A.; Figueroa-Abundiz, V.A.; Olson, M.E. The vessel wall thickness–vessel diameter relationship across woody angiosperms. Am. J. Bot. 2022, 109, 856–873. [Google Scholar] [CrossRef]
  63. Deng, C.Y.; Zheng, J.M.; Zhang, W.C.; Guo, S.Z.; Xue, Q.H.; Ye, L.Y.; Sun, J.W. Ecological wood anatomy of Rhizophora stylosa. Chin. J. Plant Ecol. 2015, 39, 604. [Google Scholar] [CrossRef]
  64. Zheng, D.; Martínez-Cabrera, H.I. Wood anatomical correlates with theoretical conductivity and wood density across China: Evolutionary evidence of the functional differentiation of axial and radial parenchyma. Ann. Bot. 2013, 112, 927–935. [Google Scholar] [CrossRef]
  65. Carlquist, S. Living cells in wood 3. overview; functional anatomy of the parenchyma network. Bot. Rev. 2018, 84, 242–294. [Google Scholar] [CrossRef]
  66. Carlquist, S. Living cells in wood. 1. Absence, scarcity and histology of axial parenchyma as keys to function. Bot. J. Linn. Soc. 2015, 177, 291–321. [Google Scholar] [CrossRef]
Water 16 03207 g001
Figure 1. Mangrove sites sampled in in the Gulf of Nicoya, Costa Rica (a), and equipment utilized for extracting increment cores from mangrove trees (b–e).
Figure 1. Mangrove sites sampled in in the Gulf of Nicoya, Costa Rica (a), and equipment utilized for extracting increment cores from mangrove trees (b–e).
Water 16 03207 g001
Water 16 03207 g002
Figure 2. Macroscopic cross-sections of species of six mangroves growing in the north Pacific of Costa Rica: (a-1–a-3) A. bicolor, (b-1–b-3) A. germinans, (c-1–c-3) L. racemosa, (d-1–d-3) P. rhizophorae, (e-1–e-3) R. mangle and (f-1–f-3) R. racemosa. Note: White arrows show black successive xylem rings alternating with the phloem and black arrow show annual ring boundary.
Figure 2. Macroscopic cross-sections of species of six mangroves growing in the north Pacific of Costa Rica: (a-1–a-3) A. bicolor, (b-1–b-3) A. germinans, (c-1–c-3) L. racemosa, (d-1–d-3) P. rhizophorae, (e-1–e-3) R. mangle and (f-1–f-3) R. racemosa. Note: White arrows show black successive xylem rings alternating with the phloem and black arrow show annual ring boundary.
Water 16 03207 g002
Water 16 03207 g003
Figure 3. Microscopic cross-sections of species of six mangroves growing in the north Pacific of Costa Rica: (a–c) Avicennia sp., (d–f) L. racemosa, (g–i) P. rhizophorae, (j–l) R. mangle and (m–o) R. racemosa. Note: White arrows show annual ring boundary.
Figure 3. Microscopic cross-sections of species of six mangroves growing in the north Pacific of Costa Rica: (a–c) Avicennia sp., (d–f) L. racemosa, (g–i) P. rhizophorae, (j–l) R. mangle and (m–o) R. racemosa. Note: White arrows show annual ring boundary.
Water 16 03207 g003
Water 16 03207 g004
Figure 4. Vessels details of six mangrove species growing in the north Pacific of Costa Rica: (a) white arrow shows scalariform perforations in R. mangle in a tree from site 1, (b) white arrow shows reticulate perforation plate in R. mangle from a tree of site 3, (c) scalariform pits present in R. mangle and R. racemosa, (d) white arrow shows gums presence in R. racemosa in tree from site 1, (e) white arrow shows intervessel pits of shape of alternate pits polygonal and vestured of L. racemosa in tree from site 3 (f,g) white arrow shows vessel-ray pitting with distinct borders: similar to intervessel pits in size and shape throughout the ray cell in A. bicolor and L. racemosa and (h) vessel-ray pits with reduced borders to apparently simple, pits horizontal (gas-like) to vertical and restricted to marginal rows in R. racemosa.
Figure 4. Vessels details of six mangrove species growing in the north Pacific of Costa Rica: (a) white arrow shows scalariform perforations in R. mangle in a tree from site 1, (b) white arrow shows reticulate perforation plate in R. mangle from a tree of site 3, (c) scalariform pits present in R. mangle and R. racemosa, (d) white arrow shows gums presence in R. racemosa in tree from site 1, (e) white arrow shows intervessel pits of shape of alternate pits polygonal and vestured of L. racemosa in tree from site 3 (f,g) white arrow shows vessel-ray pitting with distinct borders: similar to intervessel pits in size and shape throughout the ray cell in A. bicolor and L. racemosa and (h) vessel-ray pits with reduced borders to apparently simple, pits horizontal (gas-like) to vertical and restricted to marginal rows in R. racemosa.
Water 16 03207 g004
Water 16 03207 g005
Figure 5. (a,c) White arrow shows vessels grouping in clusters in sites 1 and 3 in A. germinans, respectively, (b) vessels grouping in radial multiples of four cells in site 2 in Avicennia germinans, (d) white arrow shows septate fiber presence in P. rhizophorae in site 3, (e,f) white arrow shows fiber pits in radial and tangential walls in R. racemosa in site 3 and R. mangle in site 1, and (g) white arrow shows helical thickening in vessels element in R. mangle in site 3.
Figure 5. (a,c) White arrow shows vessels grouping in clusters in sites 1 and 3 in A. germinans, respectively, (b) vessels grouping in radial multiples of four cells in site 2 in Avicennia germinans, (d) white arrow shows septate fiber presence in P. rhizophorae in site 3, (e,f) white arrow shows fiber pits in radial and tangential walls in R. racemosa in site 3 and R. mangle in site 1, and (g) white arrow shows helical thickening in vessels element in R. mangle in site 3.
Water 16 03207 g005
Water 16 03207 g006
Figure 6. (a) Rays exclusively uniseriate in P. rhizophorae in site 1, (b) ray width 1 to 3 cells in P. rhizophorae in site 3, (c) white arrow shows ray width 1–3 seriate and 4–5 seriate in A. bicolor in site 3, (d) white arrow shows ray width 4 to 10 seriate in R. mangle in site 1, (e) white arrow shows disjunctive ray parenchyma cell walls in L. racemosa in site 1, (f) white arrow shows ray with apparent disjunctive parenchyma cell walls in R. racemosa in site 1, (g) white arrow shows ray with apparent disjunctive parenchyma cell walls in P. rhizophorae in site 1, (h,i) non-crystals presence in ray cells in A. germinans in site 3 and L. racemosa in site 2, (j,k) prismatic crystals in square ray cell and procumbent ray cell in L. racemosa in trees from site 3 and A. bicolor in site 1 and (l) white arrow shows raphides crystals shape in P. rhizophorae in site 1.
Figure 6. (a) Rays exclusively uniseriate in P. rhizophorae in site 1, (b) ray width 1 to 3 cells in P. rhizophorae in site 3, (c) white arrow shows ray width 1–3 seriate and 4–5 seriate in A. bicolor in site 3, (d) white arrow shows ray width 4 to 10 seriate in R. mangle in site 1, (e) white arrow shows disjunctive ray parenchyma cell walls in L. racemosa in site 1, (f) white arrow shows ray with apparent disjunctive parenchyma cell walls in R. racemosa in site 1, (g) white arrow shows ray with apparent disjunctive parenchyma cell walls in P. rhizophorae in site 1, (h,i) non-crystals presence in ray cells in A. germinans in site 3 and L. racemosa in site 2, (j,k) prismatic crystals in square ray cell and procumbent ray cell in L. racemosa in trees from site 3 and A. bicolor in site 1 and (l) white arrow shows raphides crystals shape in P. rhizophorae in site 1.
Water 16 03207 g006
Water 16 03207 g007
Figure 7. Ray cells composition and crystals presence of six mangroves growing in the north Pacific of Costa Rica: (a) rays with procumbent, square and upright cells mixed throughout the ray in P. rhizophorae, (b): all ray cells upright and/or square in in P. rhizophorae, (c): body ray cells procumbent with mostly 2–4 rows of upright and/or square marginal cells and crystals presence in R. racemosa and (d): all body ray cells of cell procumbent in R. racemosa.
Figure 7. Ray cells composition and crystals presence of six mangroves growing in the north Pacific of Costa Rica: (a) rays with procumbent, square and upright cells mixed throughout the ray in P. rhizophorae, (b): all ray cells upright and/or square in in P. rhizophorae, (c): body ray cells procumbent with mostly 2–4 rows of upright and/or square marginal cells and crystals presence in R. racemosa and (d): all body ray cells of cell procumbent in R. racemosa.
Water 16 03207 g007
Water 16 03207 g008
Figure 8. Axial parenchyma of six mangroves growing in the north Pacific of Costa Rica: (a) white arrow shows axial parenchyma diffuse in A. bicolor in site 2, (b) white arrow shows axial parenchyma diffuse in P. rhizophorae in site 2, (c) white arrow shows axial parenchyma unilateral paratracheal in A. germinans in site 1, (d) white arrow shows axial parenchyma vasicentric and unilateral in L. racemosa in site 1, (e) white arrow shows axial parenchyma unilateral, aliform and confluent in L. racemosa in site 3, (f) white arrow shows over 8 cells per parenchyma strand in A. bicolor in site 1, (g) white arrow shows 5–8 cells per parenchyma strand in L. racemosa in site 1, (h) white arrow shows 3–4 cells per parenchyma strand in P. rhizophorae in site 1, and (i) white arrow shows 5–8 cells per parenchyma strand difficult to observe in R. mangle in site 2.
Figure 8. Axial parenchyma of six mangroves growing in the north Pacific of Costa Rica: (a) white arrow shows axial parenchyma diffuse in A. bicolor in site 2, (b) white arrow shows axial parenchyma diffuse in P. rhizophorae in site 2, (c) white arrow shows axial parenchyma unilateral paratracheal in A. germinans in site 1, (d) white arrow shows axial parenchyma vasicentric and unilateral in L. racemosa in site 1, (e) white arrow shows axial parenchyma unilateral, aliform and confluent in L. racemosa in site 3, (f) white arrow shows over 8 cells per parenchyma strand in A. bicolor in site 1, (g) white arrow shows 5–8 cells per parenchyma strand in L. racemosa in site 1, (h) white arrow shows 3–4 cells per parenchyma strand in P. rhizophorae in site 1, and (i) white arrow shows 5–8 cells per parenchyma strand difficult to observe in R. mangle in site 2.
Water 16 03207 g008
Water 16 03207 g009
Figure 9. Quantity of variation in anatomical features (a), species (b) and sites (c) of six mangroves growing in the north Pacific of Costa Rica.
Figure 9. Quantity of variation in anatomical features (a), species (b) and sites (c) of six mangroves growing in the north Pacific of Costa Rica.
Water 16 03207 g009
Table 1. Characteristics of sites studied for six tree mangroves on the Pacific coast of Costa Rica.
Table 1. Characteristics of sites studied for six tree mangroves on the Pacific coast of Costa Rica.
SiteNombreDescription
Site 1ChomesThe mangrove area is 5241.16 ha, and the dry season is from December to April, with an average annual rainfall of 73.74 mm and a rainy season from May to November with a precipitation of 1046.73 mm/year. The average annual temperature varies from 21.03 to 36.42 °C and humidity varies from 60.30% to 85.26%. The salinity is 27.05 UPS measured at a depth of 40 cm. The inundation class is type I. This site presents the influence of running water by permanent rivers or streams. The mangroves are in the coastal line (Figure 1a) and are directly influenced by the tide, and the winds also directly affect them.
Site 2RNVS CipanciThe mangrove area is 861 ha, and the dry season is from December to April, with an average annual rainfall of 73.7 mm, a rainy season from May to November, and a precipitation of 1047 mm/year. The average annual temperature varies from 21.0 to 36.4 °C, and the humidity varies from 60.3% to 85.3%. The salinity is 38.6 UPS measured at a depth of 40 cm. The inundation class is type I. This site does not present influence of running water by permanent rivers or streams and is not influenced by the ocean tide.
Site 3Río Seco ChacaritaThe mangrove area is 5241 ha and the dry season lasts six months (December to April) with an average annual rainfall of 73.7 mm and a rainy season (May to November) with 1047 mm/year. The average annual temperature varies from 21.0 to 36.4 °C and humidity varies from 60.3% to 85.3%. The salinity is 18.95 UPS measured at a depth of 40 cm. The inundation class is type I. This site does not present any influence of running water by permanent rivers or streams and is not influenced by the ocean tide.
Table 2. ANOVA of different wood properties for six different mangroves growing in the north Pacific of Costa Rica.
Table 2. ANOVA of different wood properties for six different mangroves growing in the north Pacific of Costa Rica.
ParameterSpecies EffectSite EffectInteraction
Green moisture content61.64 **0.88 NS1.86 NS
Green density25.32 **13.99 **2.5 *
Specify gravity109.93 **18.43 **3.17 **
Carbon content24.52 **8.09 *1.83 NS
Vessel diameter55.17 **9.62 **6.19 **
Length of vessel85.53 **8.57 **10.61 **
Frequency of vessel32.15 **7.04 **9.11 **
Length of fiber18.74 **13.83 **2.65 **
Diameter of fiber101.76 **0.39 NS4.28 **
Diameter of lumen187.62 **17.29 **7.71 **
Wall cell thick119.34 **11.58 **7.31 **
Ray height 76.66 **2.00 NS3.83 **
Ray width cell278.22 **183.60 **120.41 **
Note: ** statistically significant at 99% of confidence, * statistically significant at 95% of confidence and NS not statistically significant.
Table 3. Diameter, moisture content, green density, specify gravity and carbon content of six mangrove species growing in the north Pacific of Costa Rica.
Table 3. Diameter, moisture content, green density, specify gravity and carbon content of six mangrove species growing in the north Pacific of Costa Rica.
SpeciesSiteDBH (cm)Green MC (%)Green Density (g/cm3)Specify GravityCarbon Content (%)
Avicennia bicolor128.5B44.4A1.08A0.75A43.0A
222.8B48.2A1.07A0.72A39.9B
343.0A48.8A1.07A0.72A42.3A
Avicennia germinans129.0B41.2A1.13A0.80A44.0A
225.9B51.5A1.10A0.73A43.1A
338.7A53.9A1.04A0.67A42.3A
Laguncularia racemosa128.7A46.7A0.99A0.68A45.2A
223.9A42.2A0.98A0.69A43.2B
320.7A45.8A0.78B0.53B43.7B
Pelliciera rhizophorae116.8A86.2A0.97A0.52A42.7A
216.4A66.7A0.96A0.58A41.7A
330.5B74.2A0.96A0.55A42.5A
Rhizophora mangle125.8A27.1A1.14A0.90A42.9A
224.4A22.4A1.11A0.90A43.2A
326.2A27.6A1.05A0.82B43.4A
Rhizophora racemosa130.7A26.0A1.12A0.89A42.4A
226.9A28.8A1.14A0.88A43.3A
333.7A27.6A1.07B0.84B43.9A
Note: The values in parenthesis represent coefficient of variation; different letters between different species or varieties are statistically different at 99%.
Table 4. Vessel characteristics of six mangrove species growing in the north Pacific of Costa Rica.
Table 4. Vessel characteristics of six mangrove species growing in the north Pacific of Costa Rica.
SpeciesSiteVessel Characteristics
PA and VGPF
(Pores/mm2)		LV
(µm)		DV
(µm)		PP DepositsIVPVesturedVRPOther
Avicennia bicolor15–7–1120.9A283.1A69.4A13-20–22-30-
25–7–1136.9B273.4A67.2A13-20–22-30-
35–7–1118.7A258.4A63.9A13-20–22-30-
Avicennia germinans15–7–1137.9B211.1A57.9B13-20–22-30-
25–735.4B370.9B52.7B13-20–22-30-
35–7–1124.2A390.9B71.4A13-20–22-30-
Laguncularia racemosa156.2A431.4A100.1B13+22–23+30-
2510.3B428.1A83.5A13-22–23+30-
358.4A383.5A102.6B13-22–23+30-
Pelliciera rhizophorae15–1017.4A634.1A60.3A13-22-30–34-
25–1023.9B491.3B58.4A13-22-30-
35–1040.6C432.5B56.6A13-22-30-
Rhizophora mangle15–1024.5A554.2A55.4A15-20-3135
2517.0B572.3A74.3B15-20-31–3235
3527.0A435.6B69.5B15–19-20-31–3235
Rhizophora racemosa1521.5A519.2A71.4A15-20-31–3235
2513.3B588.1A65.8A15-20-31–3235
3519.9A523.3A84.1B15-20-31–3235
Note: PA = porosity arrangement, VG: vessels grouping, PF = pores frequency, LV = length of vessels, DV = diameter of vessels, PP = perforation plates, VRP = vessels–ray pitting, IVP = intervessel pit, “-” anatomical feature absent, “+” anatomical feature present, “?” unknown feature. According to IAWA class: 5: diffuse-porous, 7: vessels in diagonal and/or radial pattern, 10: Vessels in radial multiples of 4 or more common, 11: vessels clusters common, 13: Simple perforation plates, 15: Scalariform perforation plates with ≤ 10 bars, 19: Reticulate, foraminate, and/or other types of multiple perforation plates, 21: intervessel pits opposite, 20: Intervessel pits scalariform, 22: intervessel pits alternate, 23: shape of alternate pits polygonal, 30: Vessel-ray pits with distinct borders; similar to intervessel pits in size and shape throughout the ray cell, 31: Vessel-ray pits with much reduced borders to apparently simple: pits rounded or angular, 32: Vessel-ray pits with much reduced borders to apparently simple: pits horizontal (scalariform, gash-like) to vertical, 34: Vessel-ray pits unilaterally compound and coarse (over 10 μm), 35: Vessel-ray pits restricted to marginal rows (IAWA, 1989). Different letters between different species or varieties are statistically different at 99%.
Table 5. Fiber and ray parenchyma characteristics of six mangroves growing in the north Pacific of Costa Rica.
Table 5. Fiber and ray parenchyma characteristics of six mangroves growing in the north Pacific of Costa Rica.
SpeciesSiteFiberRay Parenchyma
FL
(µm)		FD (µm)LD (µm)WCT (µm)RH (µm)RW (µm)RF (ray/mm)RWC-RHCCCR(C)Other
Avicennia bicolor11068.3A19.1A6.1A6.5A491.4A35.2A26.0A97–102105–106–108137–138–141
2971.9B18.6A5.7A6.5A734.5B42.0A20.8A97–102105–106–108137–138–141
31002.8A17.3A5.8A5.7B606.7C60.7B20.8A97–98–102105–106–108137–138–141
Avicennia germinans11007.6A20.6A4.3A8.2A692.9A31.2A21.5A97–102105–106–108137–138–141
2879.7B17.6B5.8B5.9B496.9B32.3A25.6A97–102105–106–108137–138–141
3823.3B18.7B6.0B6.3B599.3A25.8B21.7A97–102105–106–108-
Laguncularia racemosa1856.4A20.2A12.2A4.0A268.2A21.6A33.6A96109-113
2878.4A22.0B7.8B7.1B231.0B17.5B30.3A96109137–138-
3771.2A23.6B12.4A5.6C190.1C13.9C44.6B96109137–138113
Pelliciera rhizophorae11070.4A34.4A19.9A7.3A724.4A23.2B30.0A96105149113?
2839.0B30.2B13.1B8.5B563.6B17.7C31.8A96105149-
3743.9B31.2B16.4C7.4A732.9A27.1A29.9A96–97105–109--
Rhizophora mangle11014.9A25.5A6.2A9.7A793.4A115.0A9.0A97–98–102104–106–107137–138113?
21060.6A26.3A4.5AB10.9A749.0A44.0B11.5B97–102104–106137–138-
31042.5A23.9A5.6A9.2A888.3A29.0C9.4A97–102104–106137–138-
Rhizophora racemosa11306.5A25.1B4.3A10.4A948.0A46.5A6.8A97–98–102104–106–107137–138113?
21044.8B29.4A4.5A12.4A851.9A45.3A8.7B97–98–102104–106–107137–138
31115.5B27.8A4.3A11.7A853.8A36.9B6.8A97–98–102104–106137–138
Note: Fiber: FL = fiber length, FD: fiber diameter, LD = lumen diameter, WCT = wall cell thickness, FC = fiber crystals, SF = septate fiber, GTF = ground tissue fiber, PFRT = fiber pits common in both radial and tangential, FS = fiber stored. Ray parenchyma: RH = ray height, RW = ray cell width, RF = ray frequency, RWC = quantity of cell in ray width, RHC = ray height in cell, CC = cellular composition, RT = ray type, RS = ray stored, R(C) = crystals present in ray, “-” anatomical feature absent, “+” anatomical feature present, “?” unknown feature. According to IAWA class: 96: rays exclusively uniseriate, 97: ray with 1 to 3 cells, 98: larger rays commonly 4- to 10-seriate, 102: ray height 1 mm, 104: all rays cell procumbent, 105: all ray cells upright and/or square, 106: body ray cells procumbent with one row of upright and/or square marginal cells, 107: body ray cells procumbent with mostly 2–4 rows of upright and/or square marginal cells, 108: body ray cells procumbent with over 4 rows of upright and/or square marginal cells, 109: rays with procumbent, square and upright cells mixed throughout the ray, 113: disjunctive ray parenchyma cell walls, 137: prismatic crystals in upright and/or square ray cells, 138: prismatic crystals in procumbent ray cells, 141: prismatic crystals in non-chambered axial parenchyma cells, 149: raphides crystal. Different letters between different species or varieties are statistically different at 99%.
Table 6. Axial parenchyma characteristics of six mangroves growing in the north Pacific of Costa Rica.
Table 6. Axial parenchyma characteristics of six mangroves growing in the north Pacific of Costa Rica.
SpeciesSiteAxial ParenchymaOther Features
ATPPTPBPCell TypeAP(C)
Avicennia bicolor1-78–79–848592–93–94?141–154133
27678–798592–93–94141133
37678–798592–93–94141133
Avicennia germinans1-78–79–848592–93141133
2-78–798592–93141–154133
3-78–79–848592–93141–154133
Laguncularia racemosa17679–81–83–84-93–94--
2-81–83-92–93--
3-81–83-92–93–94--
Pelliciera rhizophorae17678-91–92--
27678-92--
37678-92--
Rhizophora mangle1-78?-92–93?--
2-78?-*--
3-78?-*--
Rhizophora racemosa1-78?-*--
27678?-*--
3-78?-*--
Note: ATP = apotracheal parenchyma. PTP = paratracheal parenchyma. BP = banded parenchyma. AP(C) = crystals present in axial parenchyma, “-“ anatomical feature absent, “+” anatomical feature present, “?” unknown feature. * it was not possible to determine cell type. According to IAWA class: 76: axial parenchyma diffuse, 78: axial parenchyma scanty paratracheal, 79: axial parenchyma vasicentric, 80: axial parenchyma aliform, 81: axial parenchyma lozenge-aliform, 83: axial parenchyma confluent, 84: axial parenchyma unilateral paratracheal, 85: axial parenchyma bands more than three cells wide, 91: two cells per parenchyma strand, 92: four (3–4) cells per parenchyma strand, 93: eight (5–8) cells per parenchyma strand, 94: over eight cells per parenchyma strand, 133: included phloem, concentric, 141: prismatic crystals in non-chambered axial, 154: more than one crystal of about the same size per cell or chamber.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Moya, R.; Tenorio, C.; Torres-Gómez, D.; Cifuentes-Jara, M. Variation in Annual Ring and Wood Anatomy of Six Tree Mangrove Species in the Nicoya Gulf of Costa Rica. Water 2024, 16, 3207. https://doi.org/10.3390/w16223207

AMA Style

Moya R, Tenorio C, Torres-Gómez D, Cifuentes-Jara M. Variation in Annual Ring and Wood Anatomy of Six Tree Mangrove Species in the Nicoya Gulf of Costa Rica. Water. 2024; 16(22):3207. https://doi.org/10.3390/w16223207

Chicago/Turabian Style

Moya, Róger, Carolina Tenorio, Danilo Torres-Gómez, and Miguel Cifuentes-Jara. 2024. "Variation in Annual Ring and Wood Anatomy of Six Tree Mangrove Species in the Nicoya Gulf of Costa Rica" Water 16, no. 22: 3207. https://doi.org/10.3390/w16223207

APA Style

Moya, R., Tenorio, C., Torres-Gómez, D., & Cifuentes-Jara, M. (2024). Variation in Annual Ring and Wood Anatomy of Six Tree Mangrove Species in the Nicoya Gulf of Costa Rica. Water, 16(22), 3207. https://doi.org/10.3390/w16223207

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop