Environmental Parameters and Mangrove Complexity
The means of all environmental parameters measured at three sectors (45 sampling stations; nine transects), during two seasons are provided in Table 1. Salinity was the only parameter that presented significant differences between sectors (ANOVA, F = 4.49, p = 0.03) and seasons (Mann-Whitney test, U = 3.04, p = 0.003), being higher in LC (30.4 ± 4.1 psu) and during the dry season (30 ± 3.4). Regarding the other parameters evaluated, water temperature, redox potential and depth showed significant variations (p ≤ 0.05) only between seasons, while pH only showed differences between sectors. No significant differences were detected when dissolved oxygen concentrations were compared between sectors or seasons.
Variable
|
Spatiotemporal variation
|
Table 1
Average values (and standard deviation) for environmental and mangrove characteristics in three sectors of the Boca del Cielo-San José Estuary (Chiapas, Mexico). Values are based upon measurements made between May 2019 and February 2020 Ab: Avicennia bicolor, Ag: Avicennia germinans, Ce: Conocarpus erectus, Lr: Laguncularia racemosa, Rm: Rhizophora mangle
|
Lower Channel
|
Middle Channel
|
Upper Channel
|
|
Rainy
|
Dry
|
Rainy
|
Dry
|
Rainy
|
Dry
|
Environmental variables
|
|
|
|
|
|
|
Salinity (psu)
|
27.45 (1.3)
|
33.25 (1.1)
|
21.81 (1.7)
|
30.3 (1.5)
|
19.67 (1.8)
|
26.47 (2.9)
|
Dissolved oxygen (mg·L− 1)
|
2.97 (1.1)
|
3.83 (1.1)
|
3.55 (0.3)
|
3.83 (0.1)
|
3.34 (0.1)
|
3.98 (0.2)
|
Water temperature (°C)
|
31.73 (0.7)
|
30.23 (0.8)
|
32.96 (0.5)
|
30.93 (0.4)
|
31.75 (0.4)
|
29.88 (0.4)
|
pH
|
10.48 (1.7)
|
10.47 (0.5)
|
7.95 (0.2)
|
8.18 (0.3)
|
9.23 (1.1)
|
7.69 (0.2)
|
Redox potential (mV)
|
35.24 (44.4)
|
118.59 (28.8)
|
88.47 (43.8)
|
114 (4.8)
|
19.78 (15.1)
|
100.2 (83.7)
|
|
Depth (m)
|
0.46 (0.2)
|
0.37 (0.2)
|
0.55 (0.1)
|
0.46 (0.1)
|
0.52 (0.1)
|
0.33 (0.1)
|
Distance to the mouth (km)
|
3.83 (2.6)
|
10.39 (1.7)
|
22.25 (3.1)
|
Mangrove structure, microhabitat and productivity
|
|
|
Species dominance
|
Rm > Ag
|
Rm > Ag > Lr > Ab > Ce
|
Rm > Ag > Lr > Ab
|
Litterfall production (g·m2·yr− 1)
|
1698.34 (158.8)
|
1400.63 (10.16)
|
923.31 (757.5)
|
702.69 (518.4)
|
670.06 (156.5)
|
1084.97 (683.8)
|
Stilt root density (roots·m2)
|
12.6 (4.3)
|
14.73 (10.7)
|
9.2 (7.5)
|
Stilt root basal diameter (cm·m2)
|
38.27 (4.6)
|
31.25 (3.3)
|
45.35 (7.3)
|
Pneumatophore density (roots·m2)
|
1.6 (0.53)
|
23.53 (20.5)
|
18.4 (14.2)
|
Pneumatophore basal diameter (cm·m2)
|
3.08 (2.8)
|
2.65 (0.8)
|
2.76 (0.3)
|
Tree canopy height (m)
|
13.38 (2.5)
|
11.99 (1.7)
|
13.4 (1.1)
|
Tree basal area (m2·ha− 1)
|
35.19 (6.6)
|
31.29 (4.4)
|
31.86 (3.5)
|
Tree density (trees·ha− 1)
|
1499.75 (309)
|
1484.29 (667)
|
1575.83 (471.9)
|
Complexity Index
|
9.27 (4.5)
|
24.61 (8.5)
|
23.38 (5.0)
|
Ab: Avicennia bicolor, Ag: Avicennia germinans, Ce: Conocarpus erectus, Lr: Laguncularia racemosa, Rm: Rhizophora mangle
Table 2 Characterization of 25 mangrove fish species from the Boca del Cielo-San José Estuary (Chiapas, Mexico), based on their relative contribution to sectors and microhabitats, using SIMPER analyses [Percentage contributions for dissimilarity in abundance (A%), biomass (B%) and presence/absence (P/A%)] . The checklist includes numerical abundance (NA), biomass (B), ecogeographical affinity (EA), life stage (L) and spatiotemporal distribution [Lower Channel (LC), Middle Channel (MC), Upper Channel (UC), Microhabitat (MC), Rainy (R) and Dry (D)]
|
|
|
|
|
|
|
Spatiotemporal distribution
|
SIMPER
|
Species
|
NA
|
B
|
EA
|
Lower Channel
|
Middle Channel
|
Upper Channel
|
LC vs UC
|
LC vs MC
|
a vs n
|
|
|
|
|
L
|
R
|
D
|
MH
|
L
|
R
|
D
|
MH
|
L
|
R
|
D
|
MH
|
A%
|
B%
|
A%
|
B%
|
P/A%
|
Poeciliopsis fasciata
|
1334
|
480.74
|
SF
|
J, A
|
|
|
s, m
|
J, A
|
|
|
s, p, m
|
J, A
|
|
|
s, p, m
|
2.25
|
2.32
|
2.28
|
2.10
|
-
|
Poeciliopsis turrubarensis
|
1105
|
919.67
|
SF
|
J, A
|
|
|
s, m
|
J, A
|
|
|
s, p, m
|
J, A
|
|
|
s, p, m
|
2.45
|
2.61
|
-
|
2.19
|
2.17
|
Dormitator latifrons
|
822
|
12883.7
|
ER
|
J, A
|
|
|
s
|
J, A
|
|
|
s, p, m
|
J, A
|
|
|
s, p
|
3.27
|
9.14
|
3.44
|
11.98
|
3.93
|
Poecilia nelsoni
|
410
|
515.51
|
SF
|
J, A
|
|
|
s
|
J, A
|
|
|
s, m
|
J, A
|
|
|
s, p, m
|
3.22
|
2.61
|
3.64
|
3.08
|
3.95
|
Atherinella guatemalensis
|
408
|
351.39
|
ER
|
J, A
|
|
|
s
|
J, A
|
|
|
s, m
|
A
|
|
|
s
|
9.58
|
5.04
|
6.43
|
3.78
|
5.72
|
Centropomus robalito
|
231
|
1086.5
|
EU
|
J
|
|
|
s
|
J
|
|
|
s, m
|
J
|
|
|
s
|
5.18
|
6.11
|
4.75
|
5.18
|
7.30
|
Lile gracilis
|
212
|
540.85
|
ER
|
A
|
|
|
s
|
J, A
|
|
|
s, m
|
A
|
|
|
s
|
9.27
|
3.21
|
4.38
|
3.94
|
4.34
|
Eucinostumus currani
|
192
|
2373.7
|
EU
|
J, A
|
|
|
s
|
-
|
|
|
-
|
J
|
|
|
s
|
9.02
|
14.19
|
9.63
|
14.05
|
3.11
|
Mugil setosus
|
163
|
1352.6
|
EU
|
J
|
|
|
s
|
J, A
|
|
|
s, m
|
J
|
|
|
s, m
|
4.43
|
6.88
|
4.04
|
5.13
|
6.04
|
Poeciliopsis pleurospilus
|
119
|
60.12
|
SF
|
A
|
|
|
s, m
|
J, A
|
|
|
s, p
|
J, A
|
|
|
s, p, m
|
6.14
|
-
|
2.80
|
-
|
3.88
|
Gobiomorus maculatus
|
111
|
1604.1
|
ER
|
A
|
|
|
s
|
J, A
|
|
|
s, p, m
|
J, A
|
|
|
s, p, m
|
-
|
-
|
-
|
-
|
3.93
|
Diapterus brevirostris
|
97
|
405.18
|
EU
|
J, A
|
|
|
s
|
-
|
|
|
-
|
J
|
|
|
s
|
5.96
|
4.65
|
6.44
|
4.30
|
3.14
|
Lutjanus argentiventris
|
48
|
643.9
|
ES
|
J
|
|
|
s
|
J
|
|
|
s
|
J
|
|
|
s
|
5.41
|
6.05
|
5.54
|
5.98
|
4.40
|
Astatheros macracanthus
|
46
|
381.77
|
SF
|
J
|
|
|
s
|
J
|
|
|
s, m
|
J
|
|
|
s
|
4.01
|
3.02
|
2.57
|
2.19
|
5.59
|
Amphilophus trimaculatus
|
45
|
747.78
|
SF
|
J
|
|
|
s
|
J, A
|
|
|
s, m
|
J, A
|
|
|
s
|
4.14
|
3.97
|
3.53
|
4.46
|
7.30
|
Caranx caninus
|
28
|
330.63
|
EU
|
J
|
|
|
s
|
J
|
|
|
s
|
J
|
|
|
s
|
5.18
|
4.88
|
5.79
|
5.01
|
4.85
|
Lutjanus novemfasciatus
|
25
|
313.39
|
EU
|
J
|
|
|
s
|
J
|
|
|
m
|
J
|
|
|
s
|
3.24
|
3.22
|
2.90
|
2.91
|
3.14
|
Gobionellus microdon
|
22
|
225.21
|
ER
|
J
|
|
|
s, m
|
J
|
|
|
s, m
|
J
|
|
|
s, p, m
|
3.98
|
-
|
3.73
|
2.87
|
3.88
|
Ariopsis seemanni
|
19
|
68.84
|
ER
|
-
|
|
|
-
|
J
|
|
|
s, m
|
-
|
|
|
-
|
-
|
-
|
-
|
-
|
3.17
|
Ariopsis guatemalensis
|
15
|
52.12
|
ER
|
-
|
|
|
-
|
J
|
|
|
s, m
|
-
|
|
|
-
|
-
|
-
|
-
|
-
|
2.96
|
Eleotris picta
|
7
|
335.1
|
ER
|
J
|
|
|
s
|
J, A
|
|
|
m
|
J, A
|
|
|
s
|
-
|
3.28
|
-
|
3.14
|
3.11
|
Lutjanus colorado
|
6
|
140.3
|
ST
|
J
|
|
|
s
|
J
|
|
|
s
|
J
|
|
|
s
|
-
|
2.00
|
-
|
-
|
3.43
|
Citharichthys gilberti
|
4
|
266.36
|
EU
|
J
|
|
|
s
|
-
|
|
|
-
|
-
|
|
|
-
|
5.37
|
4.51
|
5.30
|
-
|
-
|
Oligoplites saurus
|
3
|
88.10
|
EU
|
J
|
|
|
s
|
-
|
|
|
-
|
-
|
|
|
-
|
2.19
|
-
|
2.15
|
-
|
-
|
Gerres simillimus
|
3
|
51.51
|
EU
|
J
|
|
|
s
|
-
|
|
|
-
|
-
|
|
|
-
|
2.49
|
-
|
2.29
|
-
|
1.91
|
+ 5 especies*
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
Cumulative contribution
|
91.90
|
91.58
|
90.43
|
90.81
|
91.25
|
|
|
|
|
|
|
|
|
|
|
|
|
Average dissimilarity
|
44.20
|
63.64
|
47.02
|
62.83
|
62.11
|
Ecogeographical Affinity: ER, Estuarine Resident; EU, Euryhaline; SF, Secondary Freshwater, ST, Stenohaline
Life stage: J, Juvenile; A, Adult
Microhabitat: s, stilt roots; m, mixed roots; p, pneumatophores
* Anableps dowii, Bathygobius andrei, Centropomus viridis, Poecilia sphenops and Arothron meleagris were recorded species that did not contribute to characterize fish assemblages among sectors or microhabitats by SIMPER analyses
The means of the structural attributes of mangroves are shown in Table 1. For all the nine transects, R. mangle was the species with the highest overall dominance (61.8%), followed by Avicennia germinans (L.) L. (20.3%), Laguncularia racemosa L. (Gaertn) (10.2%), Avicennia bicolor Standl. (6.5%) and Conocarpus erectus L. (1.1%). By sector, R. mangle was dominant in UC and MC, with 50% and 54% respectively, and in LC with 94%. No significant differences were detected in the comparisons between sectors for tree density, basal area and canopy height; however, Complexity Index values were significantly different (ANOVA, F = 5.58, p = 0.04). Regarding the microhabitat parameters, significant differences were detected in density (ANOVA, F = 10.38, p < 0.001) and basal diameter (ANOVA, F = 47.14, p < 0.0001) of pneumatophores between sectors. The highest average litterfall (1,549.5 ± 211 g m2 yr− 1) occurred in LC, detecting significant differences between sectors (Kruskal-Wallis, H = 6.35, p = 0.04). No significant differences between seasons were detected.
The PCA of the environmental and mangrove variables explained 51.3% of the variance for the two first axes (Fig. 2). This model considered seven explanatory variables, after reducing multicollinearity. The first axis contributed with 32% of the explained variance and it was strongly related (based on eigenvectors of correlation matrix) with Complexity Index (0.42), salinity (-0.4), pH (-0.37), distance to the mouth (0.35) and litterfall (-0.34); whereas the second axis contributed with 19.3% of the explained variance and better correlated with depth (0.42) and Redox potential (-0.36). The biplot revealed that sampling events from LC were closely associated in the ordination space and well segregated from the MC and UC sampling events.
Spatio-temporal Variation Of Mangrove Fish Assemblage
A total of 5,515 specimens and 30 species of fish were collected at the 45 sampling stations established in the nine transects. These species belong to 15 families, of which 76% of the total abundance corresponded to livebearers (Poeciliidae, 52%), sleeper gobies (Eleotridae, 17%) and American silversides (Atherinopsidae, 7%). The most abundant species in this study were Poeciliopsis fasciata (Meek, 1904) (San Jerónimo livebearer), Poeciliopsis turrubarensis (Meek, 1912) (barred livebearer) and Dormitator latifrons (Richardson, 1844) (Pacific fat sleeper). The total biomass was 26,304.5 g, and the highest percentage corresponding to D. latifrons (49%). Regarding its ecological category based on the degree of tolerance to salinity, we found that the euryhaline component is the best represented in the assemblage (38%), followed by the resident estuarine (28%), secondary freshwater (24%). and stenohaline (10%) components (Table 2).
The sector with the highest species richness was LC (25 species), followed by MC (22) and UC (19). A higher numerical abundance was found in LC (2,282 organisms), followed by UC (1,961 organisms) and MC (1,272 organisms); while a higher biomass also was found in LC (10,801.2 g), followed by MC (9,725.9 g) and UC (5,777.5 g). By season, 28 and 27 species were recorded for rainy and dry seasons, respectively, although the highest biomass corresponded to the rainy season (19, 214.4 g) (Fig. 3). Total richness varied according to the microhabitat: 28 species were collected at sampling stations with stilt roots, while 9 and 18 species were collected in pneumatophores and mixed roots, respectively. For all sectors, more than 52% of the collected fish were juveniles, reaching 61% in the MC, while the highest percentage of adults was found in the UC (48%) (Fig. 4a). By microhabitat, in pneumatophores a high percentage of juveniles was found, while adults prevailed in stilt roots (Fig. 4b).
The NMDS biplots showed the existence of a gradient defined mainly by spatial scale, detecting significant variations in fish assemblages between sectors throughout the annual cycle, for abundance (ANOSIM, global R = 0.835, p = 0.001) and biomass (ANOSIM, global R = 0.741, p = 0.001) (Fig. 5a-b). In the paired tests, significant and high R values (< 0.85) were obtained for UC vs. LC and MC vs. LC, indicating a higher segregation for these groups. In the case of microhabitats, a significant gradient of fish assemblages was observed depending on the microhabitat (Fig. 5c), although the low value of R indicates a lower segregation between these groups (ANOSIM, global R = 0.315, p = 0.045). However, in the paired tests, a higher segregation was detected for stilt roots and pneumatophores (R = 0.75, p = 0.01).
According to the SIMPER analysis, the average dissimilarity in abundance among sectors ranged from 44.2 to 47%, while the average dissimilarity in biomass ranged from 63.6 to 62.8%. Most of the dissimilarity in abundance and biomass between LC-UC and LC-MC was due to the species Eucinostomus currani Zahuranec, 1980 (Pacific flagfin mojarra) and Atherinella guatemalensis (Günther, 1864) (Guatemala silverside), while Centropomus robalito Jordan & Gilbert, 1882 (Yellowfin snook) had the highest percentage contribution to dissimilarity between stilt roots and pneumatophores (Table 2).
The PERMANOVA analyses detected significant differences (p ≤ 0.05) in terms of the abundance and biomass of fishes between sectors, microhabitats and seasons; the interactions of microhabitat x season, and sector x season for abundance and biomass, respectively, are also significant (Table 3). The PERMANOVA post hoc tests for abundance and biomass showed significant differences between each pair of sectors and seasons (p = 0.0001), and for microhabitat, significance was detected only between the pairs of stilt roots - mixed roots (p < 0.01) and stilt roots - pneumatophores (p = 0.0001). The microhabitat x season interaction showed significant differences between the three categories of roots for the dry season (p < 0.05), and between stilt roots-mixed roots and stilt roots-pneumatophores, only in the rainy season (p < 0.05). For the sector x season interaction, the differences between rainy and dry were only detected in the UC and the LC (p < 0.01).
Table 3
PERMANOVA and PERMDISP results based on Bray Curtis dissimilarities on fish abundance and biomass datasets in response to Sector, Microhabitat, Season and their interactions in the Boca del Cielo-San José Estuary (Chiapas, Mexico)
|
|
PERMANOVA
|
PERMDISP
|
|
Source of variation
|
d. f.
|
MS
|
F
|
P
|
F
|
P
|
Abundance
|
|
|
|
|
|
|
|
|
Sector
|
2
|
46442
|
15.2
|
0.0001*
|
8.88
|
0.003*
|
|
Microhabitat
|
2
|
17465
|
5.72
|
0.0001*
|
8.55
|
0.012*
|
|
Season
|
1
|
28601
|
9.36
|
0.0001*
|
34.67
|
0.001*
|
|
Sector x Season
|
2
|
4720.5
|
1.55
|
0.0629
|
|
|
|
Microhabitat x Season
|
2
|
4999.2
|
1.64
|
0.0498*
|
|
|
|
Residual
|
344
|
3054.5
|
|
|
|
|
Biomass
|
|
|
|
|
|
|
|
|
Sector
|
2
|
39977
|
10.5
|
0.0001*
|
4.26
|
0.049*
|
|
Microhabitat
|
2
|
20151
|
5.29
|
0.0001*
|
8.59
|
0.012*
|
|
Season
|
1
|
18341
|
4.81
|
0.0001*
|
21.75
|
0.012*
|
|
Sector x Season
|
2
|
5660.1
|
1.49
|
0.039*
|
|
|
|
Microhabitat x Season
|
2
|
4518.1
|
1.24
|
0.205
|
|
|
|
Residual
|
344
|
3808.6
|
|
|
|
|
d. f.: degrees of freedom, MS: mean square, F: pseudo-F statistic value, P: P-values by permutation |
* denotes significant P values (< 0.05) |
Relationship Between Fish Assemblages, Mangrove Complexity, And Environmental Variables
The most explanatory DistLM for fish abundance, identified 10 significant variables (p < 0.05) in the individual analysis (all variables included except "Complexity Index"), however, in the most parsimonious model, the variables of salinity, depth, stilt roots and pneumatophores together showed the highest correlation value (R2 = 0.62) (Table 4). The dbRDA diagram explained in its first two ordination axes 57.8% of the total variation; the variables selected in the DistLM showed a higher individual Pearson correlation with axis 1 (Fig. 6-A): pneumatophores (0.92), salinity (-0.81), stilt roots (-0.6) and depth (-0.54). In the case of the most explanatory DistLM for fish biomass, it identified six significant variables (p < 0.05) in the individual analysis (pneumatophores, Complexity Index, pH, distance to the mouth, salinity and productivity), and in the most parsimonious model were salinity, distance to the mouth, stilt roots, pneumatophores and productivity, which showed a higher correlation (R2 = 0.59) (Table 4). These variables showed a higher individual Pearson correlation with axis 1 of the dbRDA ordination diagram: salinity (-0.89), pneumatophores (0.85), productivity (-0.83), distance to mouth (0.69), and stilt roots (-0.66); the total variation of the ordination was explained by 49.3% in the first two axes (Fig. 6-B).
Table 4
Marginal tests and best groups of variables selected by DistLM analyses, using the BEST procedure and Bayesian Information Criterion for Bray Curtis dissimilarities on abundance and biomass datasets for fish assemblages in the Boca del Cielo-San José Estuary (Chiapas, Mexico)
|
Marginal Tests
|
Selected Models
|
|
Variables
|
SS
|
F
|
P
|
% Variation Explained
|
Selections
|
Overall Best Solution
|
Abundance
|
Salinity
|
4805.2
|
8.70
|
0.0001*
|
35
|
+Salinity
|
BIC = 116.4
|
|
Pneumatophores
|
4775.8
|
8.62
|
0.0001*
|
35
|
+ Depth
|
R2 = 0.62
|
|
Litterfall production
|
4491.7
|
7.86
|
0.0002*
|
33
|
+ Stilt roots
|
RSS = 5189.9
|
|
pH
|
4414.2
|
7.66
|
0.0001*
|
32
|
+ Pneumatophores
|
|
|
Dissolved oxygen
|
4377.8
|
7.56
|
0.0001*
|
32
|
|
|
|
Water temperatura
|
4243.1
|
7.22
|
0.0001*
|
31
|
|
|
|
Distance to the mouth inlet
|
3140.1
|
4.79
|
0.0029*
|
23
|
|
|
|
Stilt roots
|
3055
|
4.62
|
0.0051*
|
22
|
|
|
|
Depth
|
2774.1
|
4.09
|
0.0034*
|
20
|
|
|
|
Redox potential
|
2709.3
|
3.97
|
0.0072*
|
20
|
|
|
|
Complexity Index
|
775.5
|
0.96
|
0.424
|
0.1
|
|
|
Biomass
|
Pneumatophores
|
6340.3
|
4.76
|
0.001*
|
23
|
+Salinity
|
BIC = 133.1
|
|
Complexity Index
|
6326.5
|
4.75
|
0.001*
|
23
|
+ Distance to the mouth inlet
|
R2 = 0.59
|
|
pH
|
5818.7
|
4.26
|
0.002*
|
21
|
+ Stilt roots
|
RSS = 11147
|
|
Distance to the mouth inlet
|
5731
|
4.18
|
0.002*
|
21
|
+ Pneumatophores
|
|
|
Salinity
|
5526.5
|
3.99
|
0.003*
|
20
|
+ Litterfall production
|
|
|
Litterfall production
|
3672.5
|
2.45
|
0.028*
|
13
|
|
|
|
Water temperature
|
2383.4
|
1.51
|
0.147
|
0.1
|
|
|
|
Stilt roots
|
1980.3
|
1.24
|
0.266
|
0.1
|
|
|
|
Redox potential
|
1850.4
|
1.15
|
0.342
|
0.1
|
|
|
|
Depth
|
1737.6
|
1.07
|
0.355
|
0.1
|
|
|
|
Dissolved oxygen
|
1469.9
|
0.89
|
0.486
|
0.1
|
|
|
SS: sum of squares, F: pseudo-F statistic value, P: P-values by permutation, BIC: Bayesian Information Criterion, RSS: residual sum of squares |
* denotes significant P values (< 0.05) |