Understanding the biometrical dynamic of an encrusting red algae, P. fragile on a seagrass, C. nodosa in time, data of a previous unpublished study (Mutlu et al. 2014) were examined since they were sampled at five months a year (Figure 2). This guides at filling the gap of their temporal dynamic between winter and summer samplings conducted in the present study. The abundance and biomass increased slightly from January to April, and then peaked in August, followed by occurrence of decrement in November (Figure 2). The size was distributed in contrast to the temporal density of the epiphyte, and the LAI of C. nodosa did the same distribution as well (Figure 2). However, any individual of calcareous red algae on leave of P. oceanica in the Gulf of Antalya was not encountered during 2011-2012 (Mutlu et al. 2014). Coverage of P. fragile was 6.4% of leaf surface of C. nodosa on average and varied between 1.6% in March and 16.0% in August.
Distribution of Hydrolithon boreale
Hydrolithon boreale on leave of P. oceanica occurred at 25% of the total stations in winter, at 44% in summer during the present study (Figure 3). An average coverage of H. boreale was 0.12% (max: 0.75%) of leaf surface of P. oceanica. Most occurrences took place along the westernmost coast of the study area, Muğla’s coast in winter, and all coasts of three provinces in summer (Figures 3-4).
An average abundance of 41 and 49 ind/m2 on the study area (163 and 112 ind/m2 on stations where the epiphyte occurred) was estimated in winter and summer, respectively (Table 1). In winter, maximum abundance and biomass was recorded in a particular area of the Muğla’s coast where there used to be fish farms in 2000s (c.a. 2000-2005). In summer, the abundance and biomass were maximized in the easternmost location opposed to the location in winter, and were highly variable with the regions along the coast of the study area (Figures 3-4). The lowest biomass and abundance occurred along the Antalya’s coast with a few exceptions of the locations, and a moderate value was along the Muğla’s coasts.
Diameter of H. boreale’s crust was less in winter than that in winter on average, almost similar around 2.5-2.9 mm in all stations in winter while the diameter was very different in the regions of the study area (Table 1). The maximum diameter almost doubled the winter values in summer in contrast to the abundance and biomass in summer with exception of Antalya’s Gulf where the meadows were found only on the rocks (Figures 1-4). This contrast seemed to be more pronounced on soft bottom (sand and mud) and dead matte in about 2 m high.
Similar to the diameter, thicker crust of H. boreale was observed in Muğla’s coast in both winter and summer. This trend was more apparent in summer. The thickness was in similar range between winter and summer (Table 1).
Table 1 Average (Avg) and standard deviations (SD) of the biometrics of Hydrolithon boreale and LAI of Posidonia oceanica for all stations and the stations where Hydrolithon boreale was present in winter and summer.
|
On all stations
|
On only presence
|
|
TN
ind/m2
|
D
mm
|
T
mm
|
B
µg/m2
|
LAI
|
TN
ind/m2
|
D
mm
|
T
mm
|
B
µg/m2
|
Avg
|
41
|
0.57
|
0.074
|
0.171
|
1.48
|
163
|
2.23
|
0.290
|
0.671
|
SD
|
134
|
0.99
|
0.128
|
0.528
|
0.95
|
231
|
0.30
|
0.022
|
0.895
|
Avg
|
49
|
1.11
|
0.131
|
0.232
|
3.11
|
112
|
2.52
|
0.297
|
0.529
|
SD
|
136
|
1.34
|
0.148
|
0.618
|
2.18
|
188
|
0.70
|
0.017
|
0.847
|
Of the environmental parameters, sea surface SiO2 concentration was however straight-proportionally overlapped on the size of the epiphyte, but reversely on the density (abundance and biomass) depending on the size of epiphyte and LAI of P. oceanica in summer (Figure 3). The larger epiphyte carried the less abundance on a given LAI.
Epiphyte-environment relation
Biometrics of the epiphyte was correlated negatively with sea surface temperature, and positively dissolved oxygen concentrations of the near-bottom water in winter at p<0.05. However, there was a significant correlation between the biometrics and bottom type (Table 2). Sea surface temperature was negatively correlated with the diameter and oxygen positively with density variables of the epiphyte in winter.
Table 2 Spearman correlation between the biometrics of epiphyte and physical environmental parameters (see Table 6 for the abbreviations), and bottom depth (De) and type (BT) in winter. The bold values are significantly correlated at p <0.05.
|
TN
|
D
|
T
|
B
|
|
r
|
p
|
r
|
p
|
r
|
p
|
r
|
p
|
SS
|
-0.211
|
0.155
|
-0.188
|
0.205
|
-0.156
|
0.295
|
-0.213
|
0.151
|
ST
|
-0.279
|
0.057
|
-0.309
|
0.035
|
-0.267
|
0.069
|
-0.279
|
0.058
|
SpH
|
0.129
|
0.388
|
0.101
|
0.498
|
0.12
|
0.42
|
0.126
|
0.399
|
SO
|
0.303
|
0.038
|
0.278
|
0.059
|
0.281
|
0.056
|
0.302
|
0.039
|
NS
|
0.057
|
0.702
|
0.038
|
0.802
|
0.062
|
0.678
|
0.058
|
0.698
|
NT
|
-0.29
|
0.048
|
-0.305
|
0.037
|
-0.298
|
0.042
|
-0.29
|
0.048
|
NpH
|
-0.047
|
0.755
|
-0.065
|
0.664
|
-0.065
|
0.666
|
-0.052
|
0.726
|
NO
|
0.301
|
0.04
|
0.313
|
0.032
|
0.292
|
0.047
|
0.3
|
0.04
|
Sec
|
0.13
|
0.383
|
0.136
|
0.363
|
0.164
|
0.272
|
0.133
|
0.374
|
De
|
-0.119
|
0.427
|
-0.103
|
0.489
|
-0.117
|
0.434
|
-0.121
|
0.419
|
BT
|
0.4216
|
0.0032
|
0.3431
|
0.0182
|
0.3643
|
0.0118
|
0.4206
|
0.0032
|
In summer, near-bottom temperature correlated positive-significantly the density variables (abundance and biomass) of the epiphytes in contrast to that in winter. Interestingly, the biometrics was negative-significantly correlated with sea surface concentration of the SiO2, but positively with salinity of the near-bottom water (Table 3). The PO4 of the near-bottom water was positively correlated with only crust diameter at p < 0.05 (Table 3).
Table 3 Spearman correlation between the biometrics of epiphyte and physical and chemical environmental parameters (see Table 6 for the abbreviations), and bottom depth (De) and type (BT) in summer. The bold values are significantly correlated at p <0.05.
|
TN
|
D
|
T
|
B
|
|
r
|
p
|
r
|
p
|
r
|
p
|
r
|
p
|
SS
|
-0.081
|
0.424
|
-0.113
|
0.262
|
-0.108
|
0.284
|
-0.096
|
0.344
|
ST
|
0.049
|
0.626
|
-0.098
|
0.33
|
-0.011
|
0.915
|
0.046
|
0.653
|
SpH
|
0.106
|
0.295
|
0.038
|
0.704
|
0.079
|
0.437
|
0.107
|
0.289
|
NS
|
0.29
|
0.003
|
0.358
|
0
|
0.318
|
0.001
|
0.283
|
0.004
|
NT
|
0.235
|
0.019
|
0.151
|
0.134
|
0.188
|
0.061
|
0.237
|
0.018
|
NpH
|
-0.043
|
0.672
|
-0.059
|
0.558
|
-0.017
|
0.87
|
-0.029
|
0.771
|
Sec
|
-0.156
|
0.12
|
-0.08
|
0.428
|
-0.096
|
0.341
|
-0.144
|
0.153
|
De
|
-0.146
|
0.146
|
-0.18
|
0.073
|
-0.156
|
0.122
|
-0.169
|
0.093
|
BT
|
-0.0114
|
0.91
|
0.1476
|
0.1428
|
0.0614
|
0.5437
|
-0.0097
|
0.9239
|
Ssi
|
-0.342
|
0.000
|
-0.309
|
0.002
|
-0.287
|
0.004
|
-0.321
|
0.001
|
SNO3
|
-0.075
|
0.459
|
-0.074
|
0.463
|
-0.026
|
0.794
|
-0.059
|
0.560
|
SPO4
|
0.020
|
0.841
|
-0.002
|
0.981
|
-0.022
|
0.831
|
0.011
|
0.912
|
SNO2
|
-0.006
|
0.955
|
0.040
|
0.690
|
0.064
|
0.525
|
0.004
|
0.966
|
SNH4
|
-0.108
|
0.283
|
-0.088
|
0.383
|
-0.081
|
0.423
|
-0.111
|
0.270
|
SNO2+NO3
|
-0.036
|
0.722
|
0.009
|
0.925
|
0.035
|
0.728
|
-0.023
|
0.817
|
Nsi
|
-0.061
|
0.545
|
0.054
|
0.594
|
0.031
|
0.759
|
-0.050
|
0.623
|
NNO3
|
-0.130
|
0.196
|
-0.051
|
0.618
|
-0.116
|
0.249
|
-0.123
|
0.223
|
NPO4
|
0.152
|
0.131
|
0.212
|
0.034
|
0.148
|
0.143
|
0.150
|
0.136
|
NNO2
|
0.079
|
0.433
|
0.091
|
0.367
|
0.124
|
0.218
|
0.085
|
0.403
|
NNH4
|
0.042
|
0.679
|
0.086
|
0.395
|
0.095
|
0.347
|
0.043
|
0.673
|
NNO2+NO3
|
0.043
|
0.673
|
0.054
|
0.592
|
0.084
|
0.403
|
0.047
|
0.640
|
STSM
|
-0.170
|
0.091
|
-0.127
|
0.208
|
-0.116
|
0.252
|
-0.172
|
0.087
|
NTSM
|
-0.083
|
0.412
|
-0.146
|
0.148
|
-0.195
|
0.052
|
-0.088
|
0.385
|
Chl a
|
-0.147
|
0.146
|
-0.135
|
0.182
|
-0.094
|
0.352
|
-0.145
|
0.150
|
There was an obvious relationship between density and diameter of the epiphyte and the sea surface silicate (SiO2) and LAI of the meadow in summer (Figure 4). However, biometrics of the epiphyte was not significantly correlated with the LAI of P. oceanica at p < 0.05, which has brought about the multiple-regression between the variables aforementioned.
Statistics of the linear multiple-regression was given in Table 4 for the relationship between biometrics of the epiphyte and the sea surface silicate (SiO2) and LAI of the meadow in summer. To extract out the hidden variables of the LAI and SiO2 in linear relation to the biometrics, Spearman partial correlations showed that none of the variables was correlated with the biometrics at p<0.05. Multiple-linear regression showed that there was however a significant correlation only between the thickness and the LAI and SiO2 at p< 0.05 in Table 4. Regarding to the b value, the LAI affected biometrics positively, but the SiO2 negatively (Table 4).
Table 4 Linear multiple-regression constants (a; intercept, b; slope) between the biometrics of epiphyte and LAI of Posidonia oceanica and sea surface SiO2 in summer. Bold a and b values were significantly represented for the relationship and p value was significantly correlated (R2) for the multiple correlation at p < 0.05.
|
a
|
b(LAI)
|
b(SiO2)
|
Adjusted R2
|
p
|
TN
|
63.863
|
2.629
|
-5.526
|
0.01
|
0.228
|
D
|
1.447
|
-0.013
|
-0.071
|
0.03
|
0.091
|
T
|
0.170
|
0.0005
|
-0.010
|
0.06
|
0.021
|
B
|
0.304
|
0.011
|
-0.025
|
0.01
|
0.227
|
Based on all environmental variables, the abundance of the epiphyte was not partial-correlated with any of the environmental parameters. The nutrients were not partial-correlated with any of the biometrics (Table 5). Diameter, thickness and biomass were positively partial-correlated with six of the environmental parameters at p < 0.05 (Table 5). The LAI of P. oceanica was highly correlated with the biometrics of the epiphyte (Table 5).
Table 5 Partial correlation coefficients between biometrics and the environmental parameters (see Table 6 for the abbreviations) for summer samplings. Values are only correlation coefficients which were significantly partial-correlated at p < 0.05.
|
D
|
T
|
B
|
SpH
|
0.206
|
0.243
|
0.235
|
NS
|
0.229
|
0.218
|
0.200
|
NpH
|
0.211
|
0.253
|
0.246
|
STSM
|
0.302
|
0.335
|
0.327
|
NTSM
|
0.299
|
0.335
|
0.328
|
Chl a
|
0.282
|
0.320
|
0.309
|
LAI
|
0.920
|
0.929
|
0.928
|
The Generalized Additive Model (GAM) performed with all environmental parameters in summer showed that abundance (TN) of the epiphyte was positively affected first with sea surface temperature (ST), followed by the SpH, and total suspended matter (TSM) in negative way (Figure 5). The crust diameter (D) was negatively affected by the ST, and positively by the bottom depth. The biomass (B) including also contribution of crust thickness (T) was influenced with more variables compared to abundance and diameter; the SpH and NpH affected negatively and positively the biomass, respectively. These variables were followed by the SNH4 under positive influence, and the SS and NTSM under negative influence related to the biomass (Figure 5).
Eliminating this complexity derived from the effects of all the environmental variables on the biometrics, the GAM was solved for effectiveness of each of physical and chemical variables separately (Figures 6-7).
With respect to only physical environmental parameters, the abundance was positively affected by the ST, followed negatively by the SS and slightly Sec. The diameter and thickness were mostly influenced by the pH and S; the pH affected positively the size and biomass as a function of the diameter and thickness, but the salinity negatively did (Figure 6).
In terms of effect of only chemical parameters, the TN was under negative effect of the NTSM and NNO3, and followed by that under positive effect of the SPO4 and SSi. Overall, N-based nutrients affected negatively the abundance (Figure 7). The NNO2+NO3, SSi and NNO2 increased the diameter of epiphyte, and the size was reduced by the NNO3 and SNO2 (Figure 7). As occurred in the abundance, NTSM decreased the biomass, but the SSi and SNH4 increased the biomass of the epiphyte (Figure 7).
Significant part (97.5%) of the total explained variance occurred on the PCO1 to estimate the first component based and launched on the biometrics well-correlated with SSi (Table 6 and Figure 8). The density (B and TN) of the epiphyte increased with the NS and ST, and decreased with the SSi (Table 6 and Figure 8a, b, d). The distribution of the crust diameter (D) was exactly contrasted to the density of the epiphytes on the PCO (Figure 8a-c).
Table 6 Spearman correlation coefficients between the environmental parameters and the PCO solution of the biometrics.
Environmental variables
|
Abbreviations
|
PCO1
|
PCO2
|
Sea surface salinity (PSU)
|
SS
|
0.084
|
0.102
|
Sea surface temperature (oC)
|
ST
|
-0.041
|
0.177
|
Sea surface pH
|
SpH
|
-0.103
|
0.101
|
Near-bottom water salinity (PSU)
|
NS
|
-0.289
|
-0.237
|
Near-bottom water pH
|
NpH
|
0.044
|
0.038
|
Near-bottom water temperature (oC)
|
NT
|
-0.124
|
-0.127
|
Secchi disk depth (m)
|
Sec
|
0.152
|
-0.080
|
Bottom depth (m)
|
De
|
0.148
|
0.062
|
Sea surface SiO2 (µM)
|
Ssi
|
0.342
|
0.105
|
Sea surface PO4 (µM)
|
SPO4
|
-0.019
|
-0.075
|
Sea surface NH4 (µM)
|
SNH4
|
0.111
|
0.032
|
Sea surface NO2+NO3 (µM)
|
SNO2+NO3
|
0.037
|
-0.078
|
Near-bottom water SiO2 (µM)
|
Nsi
|
0.061
|
-0.192
|
Near-bottom water PO4 (µM)
|
NPO4
|
-0.157
|
-0.094
|
Near-bottom water NH4 (µM)
|
NNH4
|
-0.042
|
0.039
|
Near-bottom water NO2+NO3 (µM)
|
NNO2+NO3
|
-0.045
|
-0.011
|
Sea surface total suspended matter (mg/l)
|
STSM
|
0.170
|
-0.119
|
Near-bottom water total suspended matter (mg/l)
|
NTSM
|
0.086
|
0.117
|
Sea surface chlorophyll a (mg/l)
|
Chl a
|
0.148
|
-0.070
|
The best descriptive trait of the biometric in direct correlation with the SSi was the diameter of the epiphyte (Figure 8c, d) since the other biometrics changed dependently on LAI of its host, P. oceanica and thickness. The enlargement of the diameter was accelerated after a threshold of about 80 µM of the SSi to about 210 µM which inhibited occurrence of the epiphyte (Figure 8c, d*). This threshold could be due to action as limiting factor for SiO2 on the growth of the epiphyte.
Of the trace elements on the blades of the meadow, the Ni originated by the nature was negatively correlated with the crust biometrics of the epiphyte and LAI of P. oceanica at p < 0.05 (Table 7). Of the anthropogenic-sourced trace elements (V, Cu, Zn, As, Cd, and Pb) in the blades, Zn was negatively correlated with only diameter of the epiphyte. In the sediments, the Ni affected negatively with the TN, T, and B of the epiphyte. However, the LAI was positively correlated with all the anthropogenic-sourced trace elements. The As was positively correlated with diameter of the crust (Table 7).
Table 7 Spearman correlation coefficients between the trace elements in blades of Posidonia oceanica and its sediments, and the biometrics of the epiphyte and LAI of P. oceanica in summer. Bold coefficients are significant at p < 0.05.
|
V
|
Cr
|
Ni
|
Cu
|
Zn
|
As
|
Cd
|
Pb
|
TN
|
-0.051
|
-0.076
|
-0.318
|
-0.197
|
-0.167
|
0.080
|
-0.065
|
0.006
|
D
|
-0.154
|
-0.143
|
-0.338
|
-0.281
|
-0.302
|
0.003
|
-0.170
|
-0.016
|
T
|
-0.092
|
-0.092
|
-0.359
|
-0.228
|
-0.210
|
0.056
|
-0.099
|
0.041
|
B
|
-0.041
|
-0.065
|
-0.317
|
-0.187
|
-0.162
|
0.090
|
-0.057
|
0.027
|
LAI
|
-0.045
|
-0.076
|
-0.326
|
-0.168
|
-0.205
|
-0.177
|
-0.081
|
-0.052
|
TN
|
0.092
|
-0.184
|
-0.418
|
-0.026
|
0.020
|
0.237
|
0.149
|
0.018
|
D
|
0.211
|
0.031
|
-0.199
|
0.084
|
0.101
|
0.350
|
0.279
|
0.197
|
T
|
0.179
|
-0.087
|
-0.322
|
0.060
|
0.088
|
0.292
|
0.240
|
0.094
|
B
|
0.101
|
-0.176
|
-0.405
|
-0.020
|
0.024
|
0.232
|
0.165
|
0.035
|
LAI
|
0.463
|
0.110
|
-0.171
|
0.361
|
0.429
|
0.384
|
0.401
|
0.358
|