Abstract
Epiphytes on Posidonia oceanica play a crucial role for determination of the ecological status of marine environment in time and space besides the seagrasses alone. The study was aimed to estimate the spatiotemporal ecological status linked to variation in biometry of an epiphytic micro-calcareous red alga, Hydrolithon boreale, found on leaves of the meadow with the exclusive environmental parameters along the entire Turkish coast of the Mediterranean Sea. Collection of Posidonia oceanica samples was conducted at 64 stations in winter (December 2018–January 2019) and 112 stations in summer (June–July 2019) by SCUBA (0.4 × 0.4 m of a quadrate frame) in the infralittoral zone along the entire Turkish Mediterranean coast surrounded by the siliciclastic Taurus Mountain Range which favor growth of epiphytic micro-calcareous red algae. Percent occurrence of the epiphyte changed seasonally—lower in winter (25%) than in summer (44%). The epiphyte which is an indicator and sensitive to undisturbed marine area grew up well to 5 mm in diameter, 0.35 mm in thickness of the crust size, and was populated up to 1006 ind/m2 in summer owing to the increased utilization of the carbonate by the epiphyte with the increased water temperature. The size was contrasted to the density (abundance and biomass) in space. The biometry was significantly dependent on the siliciclastic-carbonate deposition as inferred from SiO4–Si of the water in relation to the leaf area index (LAI) of P. oceanica. Therefore, this deposition induced specimens to grow in size, followed by the reduced density concerning the N-based nutrient of the water. Further major environmental parameters which negatively affected the biometry were pH and total suspended matter of the water, analogous to turbidity. Of the trace elements, Ni was negatively correlated with the biometry, whereas the LAI was however positively correlated with all the anthropogenic-sourced trace elements (V, Cu, Zn, As, Cd, and Pb) in the leaves. Of the bottom types, the calcite rock had a higher density than the other soft bottoms in contrast to the size of the epiphyte. Future studies could be based on the present study for determination of the ecological status regarding two dominant epiphytes on leaves of two seagrasses (H. boreale on P. oceanica and partly Pneophyllum fragile on Cymodocea nodosa) found in the different environments and substrates in space and time.
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Introduction
Posidonia oceanica is an endemic species to Mediterranean Sea, and its meadows are extending to about 40 m deep (Colantoni et al. 1982; Marbà et al. 2002); its distribution is limited by low salinity and/or high temperature (Vacchi et al. 2017). Coarsely, seagrass shoot density alone determines the ecological status of the Mediterranean marine environment (UNEP/MAP-RAC/SPA 2015; Gobert et al. 2009). Beds of P. oceanica comprise the climax community in a spatial expansion process of the organisms’ establishment (Den Hartog 1977). The meadows responded differently to the different environmental parameters depending on their different parts such as below-ground or above-ground parts, e.g., leaf, leaf-related parts, and roots. Besides the water salinity, temperature, and light (Vacchi et al. 2017) as an ecological indication and interaction, the sea surface water nitrogen negatively affected the leaf width and positively affected the number of leaves per shoot (Mutlu et al. 2022). Seasonal nutrient deficiency, which reduced growth, was more pronounced in autumn, and nutrient limitations occurred in late spring and summer (Alcoverro et al. 1997; Lepoint et al. 2002). The light reaching the leaves was further blocked through the shelf-shading of the leaves and epiphytes (Via et al. 1998). The climate affects the meadows in various ways depending on both physical and chemical variables inducing changes in sea water temperature, sea level rise, modification of wave frequency and height, and ocean acidification (Bianchi et al. 2012; Planton et al. 2012; Vacchi et al. 2017). Climatic anomalies declined meadow vitality (Pergent et al. 2014). All environmental variables aforementioned are related to presence and absence of epiphytes and their diversity on the meadows (Sfriso et al. 2007; Nesti et al. 2009).
The epiphytes on the seagrass suggest ecological indications and status for the marine environments. As occurs at every taxon, the epiphytes have sensitive and tolerant species to the levels of disturbance in the marine environment (Sfriso et al. 2007, 2009). Therefore, their density (abundance and biomass) and species composition showed direction and levels of the ecological conditions. One of the sensitive seagrasses in the Mediterranean Sea is a meadow, Posidonia oceanica, and is covered by diverse epiphytes hosted on its rhizomes and leaves (Nesti et al. 2009). The epiphytes and P. oceanica together are a good combination to assess and monitor the ecological conditions in the Mediterranean Sea. The epiphytes are composed generally of their different species in the meadow (Lepoint et al. 2000, 2006). Overall, the epiphytes are an indication and intensity level of, i.e., eutrophication, productivity, herbivory, trace chemical elements, acidification, ambiance, anthropogenically, seasonality, turbidity, warming, sedimentation, hydrodynamics, and natural land sourcing around the marine environments in time and space (Bedini et al. 2003; Balata et al. 2008; Jacquemart and Demoulin 2008; Jaschinski and Sommer 2008; Baggett et al. 2010; Brahim et al. 2020). One of the epiphyte taxa which are noticed and paid attention to the calcareous species is acted as processors in the sediments (Walker and Woelkerling 1988). The most dominant encrusting species were Hydrolithon and Pneophyllum species as epiphytes on the seagrass in the Mediterranean Sea (Jacquemart and Demoulin 2008; Piazzi et al. 2000). Only these two genera species predicted reasonably most of the ecological indications (Mann 2001; Lepoint et al. 2007; Peterson et al. 2007; Tsirika et al. 2007; Mabrouk et al. 2013; Bermejo et al. 2016; Mabrouk et al. 2017; Prado 2018; Sfriso et al. 2014, 2016, 2020) since they are very sensitive to change in the environments and common in undisturbed areas (Piazzi et al. 2002; Martinez-Crego et al. 2010; Bedini and Piazzi 2012; Brahim et al. 2020). The main indication of the encrusting micro calcareous has been focused on the acidification process in relation of the carbonate to the pH in the Mediterranean Sea (e.g. Cox et al. 2015; Mutalipassi et al. 2020; Sfriso et al. 2020) due to the global warming. The targeted species in the present study, Hydrolithon spp, had the highest coverage (18–69%; Martin et al. 2008) on seagrass at a water pH of 8.1 (8.0–8.2) while there were no such epiphytes at 7.7 pH (Martin et al. 2008; Mutalipassi et al. 2020). In an undisturbed site where the NO3 and NO2 were lower and Si (OH)4 was higher, some species (Hydrolithon farinosum (J.V.Lamouroux) Penrose & Y.M.Chamberlain 1993, Fosleilla spp. and Pneophyllum fragile Kützing, 1843) of epiphytic red algae were dominant (Mabrouk et al. 2013).
Compared to the other waters of the Mediterranean Sea, meadows are less-known for their distribution and are abundant in Turkish waters (Giakoumi et al. 2013; Vacchi et al. 2017). Besides, there are some studies on their distribution on small scale from the Turkish Levant coasts, Sea of Marmara, and Black Sea (Gücü and Gücü 2002; Çirik et al. 2006; Boudouresque et al. 2012; Mutlu et al. 2022). Hydrolithon spp and P. fragile are sensitive species for undisturbed areas (Sfriso et al. 2007, 2009). A species of the present study, Hydrolithon boreale (Foslie) Y.M.Chamberlain, 1994 is one of the larger specimens of the microcalcareous red algae in terms of size of its crust (up to 2–5 mm in diameter; Reyes and Afonso-Carrillo 1995; Bradassi 2011) and has been reported here for the Turkish Mediterranean Sea. Research on invasion success and mechanisms can guide scientists to understand regulation by a complex set of factors, including biotic and abiotic features of recipient systems, disturbance regimes, and invader life traits (Sol et al. 2012). Therefore, this brings the following present study.
Regarding the ecological importance of calcareous seaweed in the marine environment and the historical lack of comprehensive information on their distribution and ecology in the Turkish waters, this study aims to provide the first baseline information on bathymetric and seasonal distribution and biometrical patterns (density and plant traits) of the H. boreale recently appeared on the leaves of P. oceanica in the infralittoral of the Turkish pristine coast, a region of the most ultra-oligotrophic waters (Sisma-Ventura et al. 2017) of the Mediterranean Sea, and to determine biometrical dynamics and the species-environment relation of the biggest microcalcareous species emphasizing the siliciclastic-carbonate deposition.
Material and methods
Study area
The study area was located in the infralittoral zone regionally limited by a bottom depth of 30 m extending occasionally to 40–43 m hereby along the southern coast of Turkey (Mutlu et al. 2020a). The area was between Taşuçu Bay, Mersin through Antalya and Datça Bay, Muğla, along three provinces (Fig. 1). The study area was restricted by Taşucu Bay in the eastern Turkish coast since there are no further locations of a meadow, P. oceanica beyond Taşucu Bay to the eastern end of the eastern Mediterranean Sea (Ergün Taşkın who researches the presence of the meadows and macrophytes by SCUBA, pers. comm.). The study area has a coastline length of about 1100 km (Fig. 1a).
The eastern half of Mersin Bay is nutritionally fed by three major (Seyhan, Ceyhan, and Göksu) rivers and is partially under influence of the Nile River (Fig. 1b). Owing to few brooks having a moderate flow rate, Antalya Bay is oligotrophic compared to Mersin Bay. Muğla’s bays and coves are devoid of rivers and brooks but are partially fed by local creeks and have undergone the effect of the Aegean Sea from east to west (Fig. 1).
The prevailing surface rim current of the Turkish Mediterranean coast was cyclonically circulated from İskenderun Bay (the easternmost Mediterranean Sea), flowed off Mersin Bay reaching Taşucu Bay, and crossed off Antalya Gulf (cape to cape, Fig. 1f) then to Rhode Island where the current is bifurcated northerly and southerly (El-Geziry and Bryden 2010). The current velocity was faster than 20 cm s−1 typical for the entire Mediterranean Sea but was generally about 50 cm s−1 on average along the Turkish Mediterranean coast (Poulain et al. 2013).
There are three main rivers with high flow rates in the easternmost of the Turkish Mediterranean coasts, which influence the coastal zone till Anamur Cape from the east by diluting the rate westward. There are many small-scale brooks along Antalya’s coast, and some creeks along Muğla’s coast (Fig. 1b). Springs of the streams were sourced through the Taurus mountain range parallel to the Turkish Mediterranean coast (Fig. 1b). The study area has been influenced by the geological structure of the mountain. The geological chronology showed that the mountain had mixed siliciclastic-carbonate during the Paleozoic, carbonate deposition during Jurassic-Cretaceous, and then shallow-water carbonates inducing deeper-water deposits during Paleocene-Eocene (Duman et al. 2017). Therefore, the streams and groundwater feed and enhance the study area with the siliciclastic-carbonate and drains of anthropogenic sources around the beds of the streams as well (Fig. 1). The flow rates of the streams and groundwater have decreased in time due to climate change and global warming.
Anthropogenic effects were present with a variety of sources as follows: marine litter, tourism, fisher, maritime activities, and trace elements (Gündoğdu and Çevik 2017; Olguner et al. 2018; Mutlu et al. 2020b; Öztürk et al. 2021). Furthermore, the study area is under influence of intensive coastal agricultural activities, particularly throughout the coast of Mersin and Antalya providences (Fig. 1f).
Sampling and field measurements
Collection of Posidonia oceanica samples was conducted in winter (December 2018/January 2019) and summer (June/July 2019) along the entire Turkish Mediterranean coast (Fig. 1) since the biometrics of the meadows was at minima in winter and at maxima in summer. Referring to the echogram of the echosounder to see absences/presence of P. oceanica on the seafloor, 64 stations were sampled by a van Veen grab (ca. 0.1 m2 at 13 stations) and SCUBA (0.4 × 0.4 m of a quadrate frame at 51 stations, and a total of 49 stations was inhabited by P. oceanica) in winter, and 112 stations (6 by a van Veen grab and 106 by SCUBA, and 103 by P. oceanica) in summer. The stations were triplicate-sampled.
Sampling bottom depth varied between 5 and 50 m but generally between 10 and 30 m at 5-m intervals because of the safety of R/V “Akdeniz Su” with a draft of 3.7 m at the shallowest waters, sometimes extending to 35–40 m. Each cruise lasted 1.5–2 months to complete the fieldwork (Fig. 1).
Some environmental parameters of water columns were measured and sampled from the surface (prefix S) and near-bottom (prefix N) waters of the stations on the board. These parameters were physical (T; temperature in °C, pH; pH, S; salinity, and O; oxygen in mg/l) using multi-parameter probes (YSI, HiTech), chemical (nutrients; NO2 + NO3–N, NH4–N, and PO4, SiO4–Si, chl a, and TSM; total suspended matter). The oxygen was measured only in winter since the oxygen probe malfunctioned in summer and the chemical parameters were sampled only in summer due to the low occurrence of the epiphyte in winter (Figs. 2 and 3). One liter of the water was filtered through CF/C for each, of the nutrients, and total suspended matter and through CF/F filters for chl a, and then all was kept in a freezer having − 20 °C on board during the field survey. Onboard, samples of the meadow were preserved in borax-buffered formaldehyde (3%) in plastic jars on the deck of the R/V “Akdeniz Su.”
Laboratory analyses
Biological materials
A total of 45 and 100 stations were analyzed for the biometry of a calcareous epiphyte, H. boreale, in winter and summer, respectively. A total of 2928 and 5028 shoots, and 11,662 and 24,509 leave of the meadows were measured for scanning the epiphyte in winter and summer, respectively. It is hereby worthy to note that sampling more than 1000 shoots is considered a destructive sampling to this sensitive species, P. oceanica. Of the epiphytes, H. boreale was majorly recorded on the leave of P. oceanica (Tables 3, 4 in Appendix). Crust diameter (D) and thickness (T, height of about cylindrical crust) of H. boreale were measured using an ocular micrometer scale under a binocular microscope. All measurements were converted to mm. The crust weight was estimated from the crust volume (cylinder) and density of calcium carbonate (2.711 kg/m3). Abundance (TA, ind/m2) and biomass (B, μg/m2) of H. boreale were calculated to value per square meter.
Environmental materials
In the laboratory, nutrients were measured following the standard procedures (APHA 1999): Ammonium (mg NH4/l), nitrate (mg NO3/l), nitrite (mg NO2/l), phosphate (mg PO4/l), and silicon dioxide (mg SiO2 /l) were measured using the methods of 4500-NH4 B, 4500 N03-E, 4500 N02-B, 4500-P E, and 4500-SiO 2 Silica, respectively (APHA 1999). The values of the nutrients were converted to a unit μM.
For estimation of total suspended solids the filtered material with the membrane was dried in an oven at 60 °C for 24 h, and then weighed. The weight of the dried empty membrane was subtracted from the total dry material weight to get the net total suspended solids. Chlorophyll a (chl-a) was measured using a method described by Lorenzen (1967). Secchi disk depth was recorded once at each station.
Statistical analyses
Of the univariate analyses, Spearman rank correlation and partial correlation were subjected to data between biometry of the epiphyte and the environmental data to estimate the hidden environmental variables. The Spearman correlation was applied between trace elements (mg/kg) in blades of P. oceanica and its sediments (Öztürk et al. 2021), the biometrics of the epiphyte, and LAI of P. oceanica to estimate the effect of anthropogenic trace elements on the biometrics. The Generalized Additive Model (GAM) was used to estimate the effect of the predicted environmental parameters (all physics, chemists and optics, and each physics, and chemists separately) on the response biometrical variables of the epiphyte for the summer survey. The univariate statistical analyses were performed using the statistical tools of MatLab (vers. 2021a, Mathworks Inc).
The following statistical analyses were designed according to the results of the univariate statistical analyses. Of the multivariate analyses, multiple regression was used to test the relationship and correlation between the biometrics of the epiphyte and LAI of P. oceanica concentration of sea surface SiO4–Si using the MatLab statistical tool. Principal Coordinate Analyses (PCO) were applied to a triangular Euclidean distance matrix of the biometry to figure out the best variable with the variation on the component, and then the PCO configuration on the axes was correlated with the environmental variables using the Spearman rank correlation for summer survey. The multivariate analyses were performed using PRIMER 6 (vers. 6.1.13) + PERMANOVA + (1.0.3.).
Results
Plant phenology
Understanding the biometrical dynamic of an encrusting red alga, P. fragile on a seagrass, C. nodosa in time, data from a previously unpublished study (Mutlu et al. 2014) were examined since they were sampled at 5 months a year (Fig. 2). This guides in 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 the occurrence of decrement in November (Fig. 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 (Fig. 2). However, any individual calcareous red alga on leaves 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 the leaf surface of C. nodosa on average and varied between 1.6% in March and 16.0% in August.
Hydrolithon boreale on leaves of P. oceanica occurred at 25% of the total stations in winter and 44% in summer during the present study (Fig. 3). Average coverage of H. boreale was 0.12% (max: 0.75%) of the 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 (Figs. 3 and 4).
An average abundance of 41 and 49 ind/m2 in 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 were recorded in a particular area of Muğla’s coast where there used to be fish farms in the 2000s (c.a. 2000–2005). In summer, the abundance and biomass were maximized in the easternmost location as opposed to the location in winter and were highly variable with the regions along the coast of the study area (Figs. 3 and 4). The lowest biomass and abundance occurred along Antalya’s coast with a few exceptions of the locations and a moderate value was along Muğla’s coasts.
The diameter of H. boreale’s crust was less in winter than that in winter on average, almost similar to 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 (Figs. 1, 2, 3, and 4). This contrast seemed to be more pronounced on soft bottom (sand and mud) and dead matte at about 2 m high.
Similar to the diameter, the thicker crust of H. boreale was observed on Muğla’s coast in both winter and summer. This trend was more apparent in summer. The thickness was in a similar range between winter and summer (Table 1).
Of the environmental parameters, sea surface SiO4–Si 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 (Fig. 3). The larger epiphyte carried less abundance on a given LAI.
However, there was a significant correlation between the biometrics and bottom type (Table 2 in Appendix). However, there was a significant correlation between the biometrics and bottom type (Table 2 in Appendix).
Environmental parameters
Overall, sea surface temperature is at minima in December–February (14–17 to 21 °C), at maxima in July (19–28 °C)–August (28–30, and to 31 °C), and decreased from eastern to western coasts of the present study area. During the present study, the salinity varied seasonally between 38 and 39 (~ 40 in August–early September). Sea surface temperature varied between 14 and 21 °C in winter and 19 and 28.8 °C in summer and salinity between 18 and ~ 40 in winter and 24 and 38.8 in summer. Maximum Secchi disk depth was recorded as 29 m in winter and 32 m in summer. Sea surface dissolved oxygen was measured in a range of 8 to 11 mg/l in winter. The pH was recorded to be 8 and 9.1 in winter and 8.5 and 9.5 in summer.
Summer sea surface nutrients were measured as follows: The nitrite varied between 0.02 and 3.96 μM (0.47 ± 0.56 μM on average ± SD), the nitrate between 0.18 and 0.03 μM (0.12 ± 0.03 μM), the ammonium between 2.44 and 531.2 μM (126.4 ± 127.2 μM), the reactive silicate between 1 and 402 μM (32.2 ± 53.4 μM), and orto-phosphate between 0.58 and 4.87 μM (2.91 ± 1.07 μM). The total suspended matter ranged from 0.02 to 1.43 mg/l and was averaged to be 0.08 ± 0.18 mg/l, and the chl-a from 0.08 to 2.87 μg/l and 0.51 ± 0.38 μg/l on average.
Anthropogenic effect of trace elements in Posidonia blades and its sediments in the present study area; the highest bioaccumulation factor in P. oceanica was calculated for Cd. Coastal waters were heavily exposed to trace elements, and significant positive correlations were detected between the anthropogenic trace element pollutants (As, Cd, Cu, Zn, Pb, and V) and natural sourced trace elements (Ni and Cr). The Mediterranean Sea coast of Turkey did not have significant levels of Zd, Cd, Cu, and Pb pollution, whereas 65% of the stations were heavily polluted with As.
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. Sea surface temperature was negatively correlated with the diameter and oxygen positively with density variables of the epiphyte in winter.
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 SiO4–Si but positively with the salinity of the near-bottom water (Table 3 in Appendix). The PO4–P of the near-bottom water was positively correlated with only crust diameter at p < 0.05 (Table 3 in Appendix).
There was an obvious relationship between the density and diameter of the epiphyte and the sea surface silicate (SiO4–Si) and LAI of the meadow in summer (Fig. 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 were given in Table 4 in Appendix for the relationship between biometrics of the epiphyte and the sea surface silicate (SiO4–Si) and LAI of the meadow in summer. To extract out the hidden variables of the LAI and SiO4–Si 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 SiO4–Si at p < 0.05 in Table 4 in Appendix. Regarding the b value, the LAI affected biometrics positively, but the SiO4–Si negatively (Table 4 in Appendix).
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 in Appendix). Diameter, thickness, and biomass were positively partial-correlated with six of the environmental parameters at p < 0.05 (Table 5 in Appendix). The LAI of P. oceanica was highly correlated with the biometrics of the epiphyte (Table 5 in Appendix).
The Generalized Additive Model (GAM) performed with all environmental parameters in summer showed that abundance (TA) of the epiphyte was positively affected first with sea surface temperature (ST), followed by the SpH, and total suspended matter (TSM) in a negative way (Fig. 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 by more variables compared to abundance and diameter; the SpH and NpH affected negatively and positively biomass, respectively. These variables were followed by the SNH4–N under the positive influence, and the SS and NTSM under the negative influence related to the biomass (Fig. 5).
Eliminating this complexity derived from the effects of all the environmental variables on the biometrics, the GAM was solved for the effectiveness of each of the physical and chemical variables separately (Figs. 6 and 7).
Concerning 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 (Fig. 6).
In terms of the effect of only chemical parameters, the TA was under the negative effect of the NTSM and NNO3–N, followed by that under the positive effect of the SPO4–P and SSiO4–Si. Overall, N-based nutrients affected negatively the abundance (Fig. 7). The NNO2 + NO3–N, SSiO4–Si, and NNO2–N increased the diameter of the epiphyte, and the size was reduced by the NNO3–N and SNO2–N (Fig. 7). As occurred in the abundance, NTSM decreased the biomass, but the SSiO4–Si and SNH4–N increased the biomass of the epiphyte (Fig. 7).
A 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 SSiO4–Si (Table 6 in Appendix and Fig. 8). The density (B and TA) of the epiphyte increased with the NS and ST and decreased with the SSiO4–Si (Table 6 in Appendix and Fig. 8a, b, d). The distribution of the crust diameter (D) was exactly contrasted to the density of the epiphytes on the PCO (Fig. 8a–c).
The best descriptive trait of the biometric in direct correlation with the SSiO4–Si was the diameter of the epiphyte (Fig. 8c, d) since the other biometrics changed dependently on the LAI of its host, P. oceanica, and thickness. The enlargement of the diameter was accelerated after a threshold of about 80 μM of the SSiO4–Si to about 210 μM which inhibited the occurrence of the epiphyte (Fig. 8c, d*). This threshold could be due to action as a 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 in Appendix). Of the anthropogenic-sourced trace elements (V, Cu, Zn, As, Cd, and Pb) in the blades, Zn was negatively correlated only with the diameter of the epiphyte. In the sediments, the Ni was affected negatively by the TA, 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 the diameter of the crust (Table 7 in Appendix).
Discussion
Of the epiphytes on P. oceanica, encrusting algae were significantly different in their distribution between leaves (Figs. 9, 10, 11 in Appendix), and rhizomes of P. oceanica and species belonging to genus Pneophyllum and Hydrolithon spp were found generally on the leaves (Nesti et al. 2009). The epiphytic assemblages were indicators of various types of natural and anthropogenic disturbances (Table 8, Figs. 12, 13 in Appendix) and occurred to grow to detect the moderate nutrient level (Balata et al. 2008). Hydrolithon spp and P. fragile are sensitive species for undisturbed areas (Sfriso et al. 2007, 2009). Average leaf coverage on P. oceanica was estimated more than 1% by the encrusting coralline algae comprising mostly H. farinosum and Pneophyllum spp (Prado et al. 2007) higher than our estimates (< 1% on average).
Plant phenology
Similar to our estimates in summer 2–threefold higher than in winter (Peterson et al. 2007; Mabrouk et al. 2015, 2017), Sfriso et al. (2020) estimated an occurrence of 41.6% of a total of 107 stations for microcalcareous epiphytic seaweeds composed majorly of Hydrolithon, Pneophyllum, and Melobesia species in the Italian coasts. In summer, the epiphytes were increased on seagrass owing to the low concentration of the nutrient induced by the leaf turnover of the seagrass which was minima in winter (Peterson et al. 2007). This brought about a difference of 20% in the occurrence of epiphytes between winter and summer (Peterson et al. 2007) similar to the difference estimated in the present study.
Encrusting algae (generally belonging to the genera Hydrolithon and Pneophyllum) dominate the epiphytic communities and occur as patches of crusts up to 3.5 mm in diameter, which vary in thickness between thin, monostromatic crusts several tens of microns thick (Beavington-Penney Simon et al. 2004): H. boreale up to 2–5 mm in diameter and up to 0.02 mm thick (Bradassi 2011; Reyes and Afonso-Carrillo 1995) and P. fragile crusts up to 700 μm and 2 mm in diameter (Kjøsterud 1997; Bradassi 2011). Our measurements fell within the above range of the crust size of the epiphyte. The epiphyte, H. boreale, was not found on blades of P. oceanica during 2011–2012 in Antalya Gulf, but P. fragile was determined on leaves of C. nodosa on an isolated island within the study area (Fig. 1c). Therefore, C. nodosa had LAI enough only for Pneophyllum fragile considering the leaf width of C. nodosa. On contrary, the richness of rhodophyta epiphytic algae was high in winter and low in spring–autumn around Canary Island where P. fragile and H. farinosum were permanent species on leaves of C. nodosa (Reyes and Sanson 1997) and on the different coasts of the Mediterranean Sea (Jacquemart and Demoulin 2008; Mabrouk et al. 2014).
With respect to the depthwise distribution of crustose macroalgae, their coverage decreased from the shallowest to the deepest station during both winter and summer (Tsirika et al. 2007). As the depth increased, increased diameter of the epiphyte limited increase in the density of epiphyte in a given LAI of P. oceanica in a matter of carrying capacity of the leaf during the present study.
Phenology-environment relation
Sensitive epiphytes were positively correlated with water transparency and the %DO (Bermejo et al. 2016) with salinity (Sfriso et al. 2017). Nevertheless, the nutrient concentrations both in the water column and surface sediments and Chl-a were negatively correlated with the sensitive taxa (Sfriso et al. 2017).
In the Mediterranean Sea, overall the decomposition of thionitrophilous taxa reduced pH values which slowed down the growth of small calcareous species such as P. fragile and Hydrolithon spp which cannot grow in poor-bad conditions (Sfriso et al. 2007, 2009, 2014). The epiphyte was affected by the pH of the water. Sfriso et al. (2020) fixed a range of pH from > 7.93 (Martin et al. 2008; Cox et al. 2015) to 8.35 for the occurrence of the calcareous seaweeds due to inhibition of utilization of HCO3 via CO2 in higher pH (Mann 2001; Martin et al. 2008; Fragoso et al. 2010; Mutalipassi et al. 2020) for growth of calcareous seaweeds in the Mediterranean Sea (Sfriso et al. 2020).
Regarding the essential nutrient concentrations, especially N-components to the marine flora, the nutrients had concentrations 2–threefold more in 2011–2012 (absent of H. boreale on leaves) than those in 2019 during the present study area (Table 8 in Appendix). The microcalcareous epiphytic seaweeds reappeared in a location classified as bad ecological conditions and status which were then recovered to healthy conditions (Sfriso et al. 2020). Besides, nutrientphilic epiphytes were producing high biomass (Balata et al. 2008). On contrary, Mabrouk et al. (2013) compared qualification and quantification of the epiphytes between the control with high water transparency and NH4–N and disturbed sites with low NO3–N and NO2–N and high Si(OH)4-Si; epiphytic red algae especially coralline algae as H. farinosum, Fosleilla spp., and P. fragile were dominant in the disturbed area in contrast to the green epiphytic algae as agreed by the other studies (Lepoint et al. 2007; Ben Brahim et al. 2010; Balata et al. 2010). Such epiphytes had tolerance to low light intensity, mostly in a shaded area (Boudouresque et al. 1984), and rapid absorption of nutrients (Lepoint et al. 2007).
The silicate was a prominent compound for the growth of the microcalcareous epiphytic seaweed on the leaves of aquatic angiosperms (Sfriso et al. 2020). The geological chronology of the study area showed that the mountain had mixed siliciclastic-carbonate, carbonate deposition, and then deeper-water deposits derived from the shallow-water carbonates in the easternmost (e.g., Duman et al. 2017), center (Ediger et al. 1997) shelf of the Turkish Mediterranean coast and the streams can bring the carbonates (Walsh-Kennedy et al. 2014; Radeff et al. 2017). The total carbonate content of the sediment in Antalya Gulf varied between 30 and 80% in both winter and summer (Fig. 13 in Appendix, from Mutlu et al. 2014). The highest carbonate contents were measured around locations where the calcite rock was found. In Finike Bay, P. oceanica did not inhabit the bottom since sediments of the Bay had low carbonate content (Appendix 12). Inherently, crustose coralline algae at low pH (mean pH 6.9) were significantly smaller and exhibited altered skeletal mineralogy (high Mg calcite to gypsum, hydrated calcium sulfate, Kamenos et al. 2016).
Besides, the trace element concentrations (As, Cd, Cr, Cu, Ni, and Pb) differentiated the density (shoot and LAI) of P. oceanica. Epiphyte biomass of mostly P. fragile and H. farinosum predominated; the higher concentration of the trace elements caused the lower density and biomass (Bedini and Piazzi 2012). Anthropogenic-sourced trace elements increased the density of P. oceanica, and a natural trace element, Ni, decreased the density and size of the epiphyte based on measurements of trace elements by Öztürk et al. (2021). Such epiphytes are classified as good ecological indicators based on the elements (Martinez-Crego et al. 2010). However, leaf epiphytes are known to be less sensitive to chemical impacts (Piazzi et al. 2004).
Conclusions
One of the sensitive species to the environmental disturbance, H. boreale recently and dominantly occurred on the blades of a Mediterranean meadow, P. oceanica along the entire Turkish Mediterranean coast. Crusts of P. fragile on leaves of C. nodosa grew up to 2.7 mm in diameter, while crust of H. boreale on leaves of P. oceanica up to 2.9 mm in winter and 4.96 mm in summer depending on space on the leaf surface. Average coverage of H. boreale was 0.12% (up to 0.75%) of the leaf surface of P. oceanica. The epiphytes were predominant in summer. The size and density (abundance and biomass) of the epiphyte were contrasted. Primarily SiO4–Si (generally landward sourced from the mountains surrounding the study area) of the water accelerated their occurrence and growth in their size, but reduced their density. Furthermore, the pH, nutrients, (especially NO2 + NO3–N), chl-a, TSM, and salinity of the water affected the quantification of these sensitive epiphytes. Besides natural and anthropogenic trace elements, bottom types significantly affected the phenological biometrics of the epiphyte. Organically loaded coastal bottom caused being devoid of the epiphyte (Fig. 12 in Appendix). Future studies could be based on the present study for water and ecological status.
Data availability
The data are not shared but the data will be available if requested by the journal.
Code availability
All software used in the present study was used with the license of each code.
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Acknowledgements
We thanked the General Directorate of Fisheries and Aquaculture—Republic of Turkey Ministry of Agriculture and Forestry to give us official permission to sample Posidonia oceanica under protection. We thanked the crew of R/V Akdeniz Su, Tunca Olguner for reviewing the English of the text, and anonymous referees for their constructive comments. The present study was funded by The Scientific and Technological Research Council of Turkey (TUBITAK) with grant no: 117Y133 and the samples collected during 2011-2012 were provided within a framework of a project funded by TUBITAK with grant no: 110Y232.
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Erhan Mutlu received funding from the Scientific and Technological Research Council of Turkey, TÜBİTAK (grant no: 117Y133 and 110Y232).
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Mutlu, E., Karaca, D., Duman, G.S. et al. Seasonality and phenology of an epiphytic calcareous red alga, Hydrolithon boreale, on the leaves of Posidonia oceanica (L) Delile in the Turkish water. Environ Sci Pollut Res 30, 17193–17213 (2023). https://doi.org/10.1007/s11356-022-23333-w
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DOI: https://doi.org/10.1007/s11356-022-23333-w