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Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy
MPB-07776; No of Pages 7 Marine Pollution Bulletin xxx (2016) xxx–xxx
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Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy T. Bacci ⁎, M. Penna, S.F. Rende, B. Trabucco, P. Gennaro, F. Bertasi, V. Marusso, L. Grossi, A.M. Cicero ISPRA - Institute for Environmental Protection and Research, via Vitaliano Brancati 48, 00144 Rome, Italy
a r t i c l e
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Article history: Received 14 January 2016 Received in revised form 31 May 2016 Accepted 2 June 2016 Available online xxxx Keywords: Posidonia oceanica Epiphytic assemblages Biotic features Environmental impact Mediterranean Sea Costa Concordia shipwreck
a b s t r a c t This research provides first information about Posidonia oceanica canopy in the area affected by Costa Concordia wreck. Percentage cover of algal and animal taxa on the leaves was estimated and biotic features of the meadow were measured in the period just after the shipwreck until its removal from the impacted site. Changes in epiphytic assemblages and some biotic features were detected in the Disturbed site compared with Control ones, highlighting effects due to the wreck presence and activities related to its removal. A temporary decrease of encrusting macroalgae and an increase of erected macroalgae and foraminifers, as well as a temporary increase of tip erosion of the canopy were detected in the Disturbed site. The obtained results were discussed and hypotheses about possible synergic effects occurred near the wreck were commented. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction Human induced pressures on coastal ecosystems affect seagrasses through both physical damage and alterations of the water and sediment quality (Orth et al., 2006; Roca et al., 2016). In this framework, the Mediterranean seagrass Posidonia oceanica (L.) Delile has been shown to be an effective bioindicator to assess the health status of marine coastal environment (Boudouresque et al., 2009; Buia et al., 2004; Montefalcone, 2009; Pergent et al., 1995). P. oceanica meadows have traditionally been considered to act as sinks for particles due to the reduction of flow velocities by the plant canopy; the canopy can slow down water currents, trapping particles, nutrients and pollutants from the water column (Gacia et al., 1999; Gacia and Duarte, 2001; Hendriks et al., 2007; Short and Short, 1984). In this regard, biotic features of P. oceanica leaves certainly reflects the physiological state of the canopy, but may also reflect the quality of the surrounding environment. Accelerated senescence, tip erosion and biometric features of the leaves may highlight possible changes in water transparency and hydrodynamic characteristics (Buia et al., 2004; Giraud, 1979; Pergent et al., 1995). Epiphytic community can be an indicator of the ecological quality of coastal waters (Piazzi et al., 2015), being more sensitive and reacting more rapidly than the host plant to alterations (Delgado et al., 1999; Giovannetti et al., 2010; Nesti et al., 2009). In this regard, increases in the epiphyte biomass, differences in their spatial heterogeneity, shifts ⁎ Corresponding author. E-mail address: [email protected] (T. Bacci).
in species composition, morphological groups and main taxonomic groups have been observed under human disturbance regimes (Balata et al., 2007; Ben Brahim et al., 2010; Martínez-Crego et al., 2010; Piazzi et al., 2004, 2015; Ruiz et al., 2001). Epiphytic composition and abundance result from the interplay between bottom-up and top-down forces (Peterson et al., 2007), as they are mainly controlled by nutrient availability, physical constraints (hydrodynamic flows, sediment features) and biological interactions such as grazing by herbivores, competition for nutrients, light and space (Bell and Hall, 1997; Lavery and Vanderklift, 2002; Neckles et al., 1993; Prado et al., 2007; Wear et al., 1999). The impact/response relationship between epiphytic community and human pressure factors have been investigated mainly in relation to the increase of nutrient availability (Balata et al., 2010; Borum, 1985; Prado et al., 2008), and to the discharge of products of specific human activities such as industrial effluents (Cambridge et al., 1986), mining wastes (Marín-Guirao et al., 2005), fish farming (Delgado et al., 1997), drilling fluids (Allen Price et al., 1986), sewage and agricultural runoff (Lapointe et al., 2004) or effluents from desalination plants (Gacia et al., 2007). Instead, there are no available data in the literature regarding possible effect of human disturbance linked to a ship disaster. The Costa Concordia ship collided with a submerged natural rocky reef close to the Giglio Island (Tuscany, Italy) and the wreck was stranded on a rocky bottom, near a slope that leads to bathymetry between 50 and 90 m. The monitoring plan was a multiannual work aimed at assessing possible impacts on the marine ecosystem due to direct effect of the shipwreck. In fact, the presence of the wreck could have been a source
http://dx.doi.org/10.1016/j.marpolbul.2016.06.012 0025-326X/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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of uncontrolled spillage of pollutant substances such as organic waste and stocks deriving from content galley, fuel and paint residues. In this context, the present study provides first data about P. oceanica leaves epiphytes and biotic features of shoots in the area affected by Costa Concordia disaster; these biological and ecological traits are commonly used as early warning indicators of environmental quality (Giovannetti et al., 2010; Leoni et al., 2006; Marbà et al., 2006; Martínez-Crego et al., 2010), but they had never been used for this purpose in a case of study of naval disaster. The aim of the study was to evaluate the possible direct effects related to the Costa Concordia event on the epiphytic assemblages and biotic features of P. oceanica canopy in the period between the time just after shipwreck until its removing from the impact site. In this regard, under the hypothesis that both epiphytic community of seagrass leaves and biotic features of shoots may change when subjected to anthropogenic stressors, we test these differences in the period investigated with an asymmetric hierarchical experimental design that enabled comparisons of disturbed and control sites.
2. Material and methods 2.1. Study area The wreck laid on a seabed that goes from 18 m to more than 40 m depth, oriented to NE, with the stern post near Punta Gabbianara and the bow continued toward the Giglio Island harbour. In this context, the activities for the removal of the wreckage have further modified the submerged and emerged landscape (Fig. 1). The shallower part of the seabed in the shipwreck area was mainly characterized by assemblages of photophilous macroalgae over a granitic basement and by P. oceanica meadow on matte, which extended from 6 m to 35 m depth. The deeper part was characterized by coralligenous assemblages. Chlorophyll-a values indicated a HIGH ecological status sensu Water Framework Directive (WFD 2000/60/CE; ARPAT, 2012). This result was also supported by the TRIX Index data (Giovanardi and Vollenweider, 2004), confirming a low trophic level of the study marine ecosystem (ARPAT, 2012).
2.2. Sampling design and data collection Three sampling sites were selected at 10 m depth along a gradient of increasing distance from the stern of Costa Concordia wreck and according to an asymmetric hierarchical experimental design. The Disturbed site (D) was located at the stern of the wreck and two Control sites (C 1 and C 2 ) were selected northwards from the wreck, at Cupa Bay and Arenella Bay (Fig. 2). Reference shores should occur on both sides of the disturbed ones to avoid spatial segregation, but in some cases this is not possible (BenedettiCecchi and Osio, 2007). The Control sites, characterized by meadows on sand or matte, were geomorphologically and ecologically similar to the Disturbed one, as they were located in enclosed bays and exposed to the same prevailing winds. In each site three sampling areas of approximately 5 × 5 m were randomly selected. Five orthotropic shoots were collected haphazardly for each area. Samples were collected by SCUBA diving just after the shipwreck (July 2012) and afterwards (March 2013, July 2013, March 2014), until its removing from the impact site (July 2014) which took place in August 2014. Samples were stored at −20 °C pending the laboratory examinations. Biotic features of shoots (including leaf surface, brown senescent tissue length, broken tips) were gathered according to Giraud (1979). Moreover, the internal side (Alcoverro et al., 2004; Casola and Scardi, 1989) of the four outer leaves in three shoots for each area were analysed for the epiphytes community. The cover percentage of algal and animal taxa of each fields of view of 1 cm 2 were estimated for each leaf under a stereo microscope, starting from the ligule up to the leaf apex. The estimates were based on the portion occupied by taxa, ideally brought together in the same segment of the leaf sensu Morri (1991). The cover percentage of the erected species was evaluated as the area occupied by their projection on portions of leaf examined. Epiphytes were analysed in accordance with the following groups: encrusting algae, erected algae (in this group the non-calcified Ochrophyta Myrionema spp. is included given its ecological relevance with epiphytic associations of mature assemblages), bryozoans, hydroids, foraminifers, spirorbids and ascidians.
Fig. 1. Panoramic view of the Disturbed site. a) Just after the shipwreck (March 13th, 2012); b) before the parbuckling of the wreck (August 8th, 2013); c) after the parbuckling and before the removal of the wreck from the site (September 19th, 2013).
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
T. Bacci et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
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Fig. 2. Location of the study area. Disturbed site (D) (42°21′59.64″ N; 10°55′13.57″ E); Control sites (C1 and C2) (42°22′05.59″ N; 10°55′04.65″ E and 42°22′10.78″ N; 10°54′51.03″ E).
2.3. Data analysis Multivariate analysis of variance based on permutations (PERMANOVA, Anderson, 2001) was performed to examine differences in patterns of composition and abundance of epiphyte among sampling sites. The analysis consisted in a three-way mixed model with Site (3 levels) as fixed and Time (5 levels) as random and orthogonal factors, Area (3 levels) as random factor nested in Site. As most of the impact studies, statistical analyses were asymmetrical as only one Disturbed site was fixed (Glasby, 1997; Underwood, 1992). PERMANOVA was performed on the basis of Bray–Curtis measures of dissimilarity (Bray and Curtis, 1957) using untransformed data. Data were averaged across leaves so that shoots provided replicates in the analyses. The sums of squares of factor Site were divided into two components: the contrast Disturbed versus Control (D vs C) and the variability between Controls (C1 vs C2) (Terlizzi et al., 2005). P-value was performed on PERMANOVA (perm) or Monte Carlo (MC) methods with few (b 100) unique permutations (Anderson et al., 2008). Homogeneity of multivariate dispersions was verified with PERMDISP (Anderson, 2006) to test the robustness of PERMANOVA analysis respect to sample dispersion (Anderson et al., 2008). Data were graphically represented using nonmetric Multi-Dimensional Scaling (nMDS) ordination. PERMANOVA and PERMDISP analysis were also used as univariate tests (ANOVA and Levene's test respectively) in order to detect possible differences between Disturbed and Control sites of total epiphyte cover, total cover of algae and animals, cover of each group and in biotic features of P. oceanica (including leaf surface, brown senescent tissue length, broken tips) of intermediate and adult leaves sensu Giraud (1979). The procedure was based on Euclidean distance using untransformed data and the partitioning of the total variation, in among-group and within-group sums of squares, was constructed in the same way as multivariate tests (Anderson et al., 2008). Statistical analyses were performed using PERMANOVA+ for PRIMER software (version 1.0.1; Anderson et al., 2008).
3. Results Multivariate analysis detected significant differences in the epiphyte assemblages between Disturbed and Control sites limited to some
sampling dates while there was no evidence of differences between the two Control sites (Table 1). In this regard, the nMDS ordination plot of the epiphyte assemblages shown a slight separation between Disturbed and Control sites for all sampling dates, which lay above and below of the plot respectively (Fig. 3). Univariate analysis showed similar results in the total epiphyte cover (TixDvsC P b 0.0062) and in the total algae epiphyte cover (TixDvsC P b 0.001) between Disturbed and Control sites, highlighting lower mean value and higher mean value in Disturbed site in July 2012 and March 2014 respectively, while no significant differences between Disturbed and Control sites were detected in total animals epiphyte cover (Fig. 4). With regard to the groups of organisms, encrusting algae, erected algae and bryozoans were almost always common at all sites. Also hydroids, foraminifers, spirorbids and ascidians were widespread in all sites, but their mean percentage cover was generally lower than other taxa (Fig. 5). Univariate analysis indicated significant differences between Disturbed and Control sites for encrusting algae (TixDvsC P b 0.0001), highlighting mean lower values of cover in Disturbed site in July 2012 (Fig. 5). Significant differences between Disturbed and Table 1 Multivariate analysis (PERMANOVA) on epiphyte assemblages of Posidonia oceanica leaves (July 2012, March 2013, July 2013, March 2014, July 2014). Bold numbers indicate significant effects. Si = Site; DvsC = Disturbed vs Control; C = Control1 vs Control2; Ti = Time; Ar = Area. Source of variability
df
MS
Pseudo-F
P (perm)
Si
2 1 1 4 6 4 4 8 4 4 24 16 16 90 134
2399.8 3609.9 1189.7 3892.9 1438.6 1252.4 1364.2 1896.5 2798.2 994.89 953.62 921.91 1028.4 550.82
1.005 1.132 0.940 4.082 1.509 1.358 1.327 1.989 3.144 0.967 1.731 1.456 1.822
0.4713 0.3716 0.5245 0.0001 0.1010 0.1996 0.2278 0.0111 0.0020 0.4906 0.0011 0.0294 0.0018
DvsC C Ti Ar(Si) Ar(DvC) Ar(C) Ti × Si Ti × DvC Ti × C Ti × Ar(Si) Ti × Ar(DvC) Ti × Ar(C) Res Total
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 3. nMDS ordination plot (3D) of epiphytic assemblages of leaves in Disturbed (D) and Control (C1 and C2) sites (July 2012, March 2013, July 2013, March 2014, July 2014). M = March; J = July; 12 = 2012; 13 = 2013; 14 = 2014.
Control sites were highlighted also for erected algae (DvsC P b 0.0147) and foraminifers (DvsC P b 0.0096), with mean higher values in Disturbed site compared with Control ones, especially from 2013 onwards
(Fig. 5). Only PERMDISP results obtained for foraminifers cover indicated a significant dispersion among samples (P b 0.001). No significant differences between Disturbed and Control sites occurred for hydroids, bryozoans, spirorbids and ascidians cover. Moreover, there was no evidence of differences between the two Control sites for any of the taxa considered (Fig. 5). The analysis detected significant higher values for broken tips in Disturbed site than in the Control sites (TixDvsC P b 0.03), especially in July 2013 and July 2014, while no significant evidence of differences occurred for leaf surface and brown senescence tissue length between sites. Similarly, there were no differences between the two Control sites for any of these biotic variables (Fig. 6). 4. Discussion
Fig. 4. Mean (±s.e.) percentage cover of total algae and total animals in Disturbed (D) and Control (C1 and C2) sites (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; ***P b 0.001).
Effects of Costa Concordia event on P. oceanica canopy were detected. Evidence of differences on epiphytic assemblages and some biotic features of leaves was found between Control sites and Disturbed site, where disturbance signals on macrostructure of the meadow were also identified (personal observation). Conversely, epiphytic assemblages and canopy biotic traits remained unchanged between the Control sites throughout the whole study period, confirming a correct selection of the reference sites for this case of study. With regard to the epiphytic community of P. oceanica leaves, the analysis carried out on the macroalgal assemblages highlighted that crustose coralline algae was the group of algae most threatened by the wreck of Costa Concordia, at least in the first period after the naval disaster. These organisms, belonging to the genera Hydrolithon (Foslie) Foslie, 1909 and Pneophyllum Kutzing, 1843, generally dominated and characterized most of the leaf surfaces, according to the oligotrophic characteristics of water column investigated, where the epiphytic assemblage is generally dominated by crustose coralline algae (Keuskamp, 2004). Decrease of coralline algae in our data mirrored
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 5. Mean (±s.e.) percentage cover of each epiphyte group in Disturbed (D) and Control sites (C1 and C2) (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; **P b 0.01).
other results (Balata et al., 2007; Martínez-Crego et al., 2010) in a moderately disturbed P. oceanica meadow. However, lack of differences between Disturbed and Control sites from March 2013 onwards highlights temporary effects on these species and a fast recovery of these encrusting assemblages. Differently, higher cover of erected macroalgae was detected near the wreck, mainly represented by brown algae of the epiphytic
association Myrionemo-Giraudietum sphacelarioidis Van der Ben 1971, which generally typify an epiphytic community in its mature stage (Casola et al., 1987). Our findings show effects on erected macroalgae, especially from July 2013 onwards, when the presence of the wreck together with the yard and related activities have completely changed the natural characteristics of the original site, suggesting the occurrence of disturbances in continuous evolution. In this regard, in fact, brown
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 6. Mean (±s.e.) of selected biometric features in Disturbed (D) and Control sites (C1 and C2) (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; **P b 0.01; ***P b 0.001).
algae have been shown to be favored with respect to the other functional components of the epiphyte community in condition of a moderate nutrient increase because of their faster-growing ecology (Lepoint et al., 2007). With regard to the faunal assemblages, the increase of foraminifers abundance on P. oceanica leaves, as well as the increase of their variance in the site near the wreck from March 2013 onwards, does not seem to find an easy explanation since no similar evidence in the literature is known. Epiphytic foraminiferal populations usually respond to nutrient enrichment with a decrease in abundance, thus they may be useful indicators of ecosystem decline in subtropical–tropical, oligotrophic marine habitats (Richardson, 2006). Although these protozoans in surface sediments colonized by P. oceanica have been shown to be useful indicators to characterize a given environment in an integrated way (MateuVicens et al., 2014), no information is reported about the possible significant changes of foraminifers in leaf epiphytic assemblages colonizing disturbed meadows of P. oceanica (Piazzi et al., 2015). Therefore, further investigations should be carried out on the use of this taxon as bioindicator in epiphytic community studies on P. oceanica. However, changes in foraminifers abundance, as well as differences in their patterns of distribution and each other difference between
Disturbed and Control sites may have been due to other source of disturbance existing in the site near the wreck. In fact, Costa Concordia wreck acted as an artificial reef, forming a large additional submerged solid substrate (about 10,000 m2) subjected to fouling attack. Settlement and growth of marine plants and animals on the wreck may have interacted with the epiphytic community of the neighboring meadow. In this regard, distance from rocky reefs has been shown to have a direct influence on the structure of adjacent epiphytic assemblages (Van Elven et al., 2004). In addition, water motion which probably occurred near the wreck has been shown to be an important parameter in the epiphytes colonization (Fresi et al., 1982; Kendrick and Burt, 1997), especially where water turbulence can affect the availability of potential preys such as zooplankton and particulate matter for suspension feeders (McKinney and Jackson, 1989; Wahl, 1989). The level of confinement in the Disturbed site, which was changed through time firstly with the sinking of the ship and secondly with construction of the yard for the ship removal, may have had a bearing on local hydrodynamics, promoting partly the tip erosion of the canopy, especially in the summertime in the more advanced period of the study. In addition, although no significant differences occurred for senescence tissue length, a higher mean value in the Disturbed site than in the Control sites occurred in July 2012 representing a stress marker of the meadow near the wreck. The different confinement of the Disturbed site due to the presence of the wreck, and the effects of snatchy spills just after the Costa Concordia accident, or a combined effect of both, could justify the enhanced tip senescence in the summer, when the leaf growth was in its mature stage, and the plant still was not accustomed to the new conditions. In conclusion, our results show effects of Costa Concordia event both on epiphytic assemblages and biotic features of P. oceanica canopy, suggesting however a reduced influence of the chemical pollution, as also confirmed by results of studies carried out on biomarkers Mytilus galloprovincialis in the same study area (Regoli et al., 2014). According to these results, serious contamination events or consistent increase of environmental pollution should be excluded as only some episodic spills with reversible effects emerged (Regoli et al., 2014). Moreover, structure of the canopy and its epiphytic assemblages could have been affected by synergic effects among factors associated with the body of the wreck and those related to the removal yard, where the first could have acted as a physical barrier to the natural hydrodynamics of the area, changing significantly the submerged landscape of the Disturbed site. Acknowledgements The Monitoring Plan was founded by the Italian National Civil Protection Agency in the framework of the Costa Concordia accident emergency. References Alcoverro, T., Pérez, M., Romero, J., 2004. Importance of within-shoot epiphyte distribution for the carbon budget of seagrasses: the example of Posidonia oceanica. Bot. Mar. 47. http://dx.doi.org/10.1515/BOT.2004.036. Allen Price, W., Macauley, J.M., Clark, J.R., 1986. Effects of drilling fluids on Thalassia testudinum and its epiphytic algae. Environ. Exp. Bot. 26, 321–330. http://dx.doi. org/10.1016/0098-8472(86)90019-5. Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46. http://dx.doi.org/10.1111/j.1442-9993.2001.01070.pp.x. Anderson, M.J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253. http://dx.doi.org/10.1111/j.1541-0420.2005.00440.x. Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. 2008. ARPAT, 2012. Monitoraggio della qualità ambientale nell'area interessata dall'incidente della nave Costa Concordia. Report. p. 71. Balata, D., Nesti, U., Piazzi, L., Cinelli, F., 2007. Patterns of spatial variability of seagrass epiphytes in the north-west Mediterranean Sea. Mar. Biol. 151, 2025–2035. http://dx. doi.org/10.1007/s00227-006-0559-y.
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Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy T. Bacci ⁎, M. Penna, S.F. Rende, B. Trabucco, P. Gennaro, F. Bertasi, V. Marusso, L. Grossi, A.M. Cicero ISPRA - Institute for Environmental Protection and Research, via Vitaliano Brancati 48, 00144 Rome, Italy
a r t i c l e
i n f o
Article history: Received 14 January 2016 Received in revised form 31 May 2016 Accepted 2 June 2016 Available online xxxx Keywords: Posidonia oceanica Epiphytic assemblages Biotic features Environmental impact Mediterranean Sea Costa Concordia shipwreck
a b s t r a c t This research provides first information about Posidonia oceanica canopy in the area affected by Costa Concordia wreck. Percentage cover of algal and animal taxa on the leaves was estimated and biotic features of the meadow were measured in the period just after the shipwreck until its removal from the impacted site. Changes in epiphytic assemblages and some biotic features were detected in the Disturbed site compared with Control ones, highlighting effects due to the wreck presence and activities related to its removal. A temporary decrease of encrusting macroalgae and an increase of erected macroalgae and foraminifers, as well as a temporary increase of tip erosion of the canopy were detected in the Disturbed site. The obtained results were discussed and hypotheses about possible synergic effects occurred near the wreck were commented. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction Human induced pressures on coastal ecosystems affect seagrasses through both physical damage and alterations of the water and sediment quality (Orth et al., 2006; Roca et al., 2016). In this framework, the Mediterranean seagrass Posidonia oceanica (L.) Delile has been shown to be an effective bioindicator to assess the health status of marine coastal environment (Boudouresque et al., 2009; Buia et al., 2004; Montefalcone, 2009; Pergent et al., 1995). P. oceanica meadows have traditionally been considered to act as sinks for particles due to the reduction of flow velocities by the plant canopy; the canopy can slow down water currents, trapping particles, nutrients and pollutants from the water column (Gacia et al., 1999; Gacia and Duarte, 2001; Hendriks et al., 2007; Short and Short, 1984). In this regard, biotic features of P. oceanica leaves certainly reflects the physiological state of the canopy, but may also reflect the quality of the surrounding environment. Accelerated senescence, tip erosion and biometric features of the leaves may highlight possible changes in water transparency and hydrodynamic characteristics (Buia et al., 2004; Giraud, 1979; Pergent et al., 1995). Epiphytic community can be an indicator of the ecological quality of coastal waters (Piazzi et al., 2015), being more sensitive and reacting more rapidly than the host plant to alterations (Delgado et al., 1999; Giovannetti et al., 2010; Nesti et al., 2009). In this regard, increases in the epiphyte biomass, differences in their spatial heterogeneity, shifts ⁎ Corresponding author. E-mail address: [email protected] (T. Bacci).
in species composition, morphological groups and main taxonomic groups have been observed under human disturbance regimes (Balata et al., 2007; Ben Brahim et al., 2010; Martínez-Crego et al., 2010; Piazzi et al., 2004, 2015; Ruiz et al., 2001). Epiphytic composition and abundance result from the interplay between bottom-up and top-down forces (Peterson et al., 2007), as they are mainly controlled by nutrient availability, physical constraints (hydrodynamic flows, sediment features) and biological interactions such as grazing by herbivores, competition for nutrients, light and space (Bell and Hall, 1997; Lavery and Vanderklift, 2002; Neckles et al., 1993; Prado et al., 2007; Wear et al., 1999). The impact/response relationship between epiphytic community and human pressure factors have been investigated mainly in relation to the increase of nutrient availability (Balata et al., 2010; Borum, 1985; Prado et al., 2008), and to the discharge of products of specific human activities such as industrial effluents (Cambridge et al., 1986), mining wastes (Marín-Guirao et al., 2005), fish farming (Delgado et al., 1997), drilling fluids (Allen Price et al., 1986), sewage and agricultural runoff (Lapointe et al., 2004) or effluents from desalination plants (Gacia et al., 2007). Instead, there are no available data in the literature regarding possible effect of human disturbance linked to a ship disaster. The Costa Concordia ship collided with a submerged natural rocky reef close to the Giglio Island (Tuscany, Italy) and the wreck was stranded on a rocky bottom, near a slope that leads to bathymetry between 50 and 90 m. The monitoring plan was a multiannual work aimed at assessing possible impacts on the marine ecosystem due to direct effect of the shipwreck. In fact, the presence of the wreck could have been a source
http://dx.doi.org/10.1016/j.marpolbul.2016.06.012 0025-326X/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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T. Bacci et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
of uncontrolled spillage of pollutant substances such as organic waste and stocks deriving from content galley, fuel and paint residues. In this context, the present study provides first data about P. oceanica leaves epiphytes and biotic features of shoots in the area affected by Costa Concordia disaster; these biological and ecological traits are commonly used as early warning indicators of environmental quality (Giovannetti et al., 2010; Leoni et al., 2006; Marbà et al., 2006; Martínez-Crego et al., 2010), but they had never been used for this purpose in a case of study of naval disaster. The aim of the study was to evaluate the possible direct effects related to the Costa Concordia event on the epiphytic assemblages and biotic features of P. oceanica canopy in the period between the time just after shipwreck until its removing from the impact site. In this regard, under the hypothesis that both epiphytic community of seagrass leaves and biotic features of shoots may change when subjected to anthropogenic stressors, we test these differences in the period investigated with an asymmetric hierarchical experimental design that enabled comparisons of disturbed and control sites.
2. Material and methods 2.1. Study area The wreck laid on a seabed that goes from 18 m to more than 40 m depth, oriented to NE, with the stern post near Punta Gabbianara and the bow continued toward the Giglio Island harbour. In this context, the activities for the removal of the wreckage have further modified the submerged and emerged landscape (Fig. 1). The shallower part of the seabed in the shipwreck area was mainly characterized by assemblages of photophilous macroalgae over a granitic basement and by P. oceanica meadow on matte, which extended from 6 m to 35 m depth. The deeper part was characterized by coralligenous assemblages. Chlorophyll-a values indicated a HIGH ecological status sensu Water Framework Directive (WFD 2000/60/CE; ARPAT, 2012). This result was also supported by the TRIX Index data (Giovanardi and Vollenweider, 2004), confirming a low trophic level of the study marine ecosystem (ARPAT, 2012).
2.2. Sampling design and data collection Three sampling sites were selected at 10 m depth along a gradient of increasing distance from the stern of Costa Concordia wreck and according to an asymmetric hierarchical experimental design. The Disturbed site (D) was located at the stern of the wreck and two Control sites (C 1 and C 2 ) were selected northwards from the wreck, at Cupa Bay and Arenella Bay (Fig. 2). Reference shores should occur on both sides of the disturbed ones to avoid spatial segregation, but in some cases this is not possible (BenedettiCecchi and Osio, 2007). The Control sites, characterized by meadows on sand or matte, were geomorphologically and ecologically similar to the Disturbed one, as they were located in enclosed bays and exposed to the same prevailing winds. In each site three sampling areas of approximately 5 × 5 m were randomly selected. Five orthotropic shoots were collected haphazardly for each area. Samples were collected by SCUBA diving just after the shipwreck (July 2012) and afterwards (March 2013, July 2013, March 2014), until its removing from the impact site (July 2014) which took place in August 2014. Samples were stored at −20 °C pending the laboratory examinations. Biotic features of shoots (including leaf surface, brown senescent tissue length, broken tips) were gathered according to Giraud (1979). Moreover, the internal side (Alcoverro et al., 2004; Casola and Scardi, 1989) of the four outer leaves in three shoots for each area were analysed for the epiphytes community. The cover percentage of algal and animal taxa of each fields of view of 1 cm 2 were estimated for each leaf under a stereo microscope, starting from the ligule up to the leaf apex. The estimates were based on the portion occupied by taxa, ideally brought together in the same segment of the leaf sensu Morri (1991). The cover percentage of the erected species was evaluated as the area occupied by their projection on portions of leaf examined. Epiphytes were analysed in accordance with the following groups: encrusting algae, erected algae (in this group the non-calcified Ochrophyta Myrionema spp. is included given its ecological relevance with epiphytic associations of mature assemblages), bryozoans, hydroids, foraminifers, spirorbids and ascidians.
Fig. 1. Panoramic view of the Disturbed site. a) Just after the shipwreck (March 13th, 2012); b) before the parbuckling of the wreck (August 8th, 2013); c) after the parbuckling and before the removal of the wreck from the site (September 19th, 2013).
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 2. Location of the study area. Disturbed site (D) (42°21′59.64″ N; 10°55′13.57″ E); Control sites (C1 and C2) (42°22′05.59″ N; 10°55′04.65″ E and 42°22′10.78″ N; 10°54′51.03″ E).
2.3. Data analysis Multivariate analysis of variance based on permutations (PERMANOVA, Anderson, 2001) was performed to examine differences in patterns of composition and abundance of epiphyte among sampling sites. The analysis consisted in a three-way mixed model with Site (3 levels) as fixed and Time (5 levels) as random and orthogonal factors, Area (3 levels) as random factor nested in Site. As most of the impact studies, statistical analyses were asymmetrical as only one Disturbed site was fixed (Glasby, 1997; Underwood, 1992). PERMANOVA was performed on the basis of Bray–Curtis measures of dissimilarity (Bray and Curtis, 1957) using untransformed data. Data were averaged across leaves so that shoots provided replicates in the analyses. The sums of squares of factor Site were divided into two components: the contrast Disturbed versus Control (D vs C) and the variability between Controls (C1 vs C2) (Terlizzi et al., 2005). P-value was performed on PERMANOVA (perm) or Monte Carlo (MC) methods with few (b 100) unique permutations (Anderson et al., 2008). Homogeneity of multivariate dispersions was verified with PERMDISP (Anderson, 2006) to test the robustness of PERMANOVA analysis respect to sample dispersion (Anderson et al., 2008). Data were graphically represented using nonmetric Multi-Dimensional Scaling (nMDS) ordination. PERMANOVA and PERMDISP analysis were also used as univariate tests (ANOVA and Levene's test respectively) in order to detect possible differences between Disturbed and Control sites of total epiphyte cover, total cover of algae and animals, cover of each group and in biotic features of P. oceanica (including leaf surface, brown senescent tissue length, broken tips) of intermediate and adult leaves sensu Giraud (1979). The procedure was based on Euclidean distance using untransformed data and the partitioning of the total variation, in among-group and within-group sums of squares, was constructed in the same way as multivariate tests (Anderson et al., 2008). Statistical analyses were performed using PERMANOVA+ for PRIMER software (version 1.0.1; Anderson et al., 2008).
3. Results Multivariate analysis detected significant differences in the epiphyte assemblages between Disturbed and Control sites limited to some
sampling dates while there was no evidence of differences between the two Control sites (Table 1). In this regard, the nMDS ordination plot of the epiphyte assemblages shown a slight separation between Disturbed and Control sites for all sampling dates, which lay above and below of the plot respectively (Fig. 3). Univariate analysis showed similar results in the total epiphyte cover (TixDvsC P b 0.0062) and in the total algae epiphyte cover (TixDvsC P b 0.001) between Disturbed and Control sites, highlighting lower mean value and higher mean value in Disturbed site in July 2012 and March 2014 respectively, while no significant differences between Disturbed and Control sites were detected in total animals epiphyte cover (Fig. 4). With regard to the groups of organisms, encrusting algae, erected algae and bryozoans were almost always common at all sites. Also hydroids, foraminifers, spirorbids and ascidians were widespread in all sites, but their mean percentage cover was generally lower than other taxa (Fig. 5). Univariate analysis indicated significant differences between Disturbed and Control sites for encrusting algae (TixDvsC P b 0.0001), highlighting mean lower values of cover in Disturbed site in July 2012 (Fig. 5). Significant differences between Disturbed and Table 1 Multivariate analysis (PERMANOVA) on epiphyte assemblages of Posidonia oceanica leaves (July 2012, March 2013, July 2013, March 2014, July 2014). Bold numbers indicate significant effects. Si = Site; DvsC = Disturbed vs Control; C = Control1 vs Control2; Ti = Time; Ar = Area. Source of variability
df
MS
Pseudo-F
P (perm)
Si
2 1 1 4 6 4 4 8 4 4 24 16 16 90 134
2399.8 3609.9 1189.7 3892.9 1438.6 1252.4 1364.2 1896.5 2798.2 994.89 953.62 921.91 1028.4 550.82
1.005 1.132 0.940 4.082 1.509 1.358 1.327 1.989 3.144 0.967 1.731 1.456 1.822
0.4713 0.3716 0.5245 0.0001 0.1010 0.1996 0.2278 0.0111 0.0020 0.4906 0.0011 0.0294 0.0018
DvsC C Ti Ar(Si) Ar(DvC) Ar(C) Ti × Si Ti × DvC Ti × C Ti × Ar(Si) Ti × Ar(DvC) Ti × Ar(C) Res Total
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 3. nMDS ordination plot (3D) of epiphytic assemblages of leaves in Disturbed (D) and Control (C1 and C2) sites (July 2012, March 2013, July 2013, March 2014, July 2014). M = March; J = July; 12 = 2012; 13 = 2013; 14 = 2014.
Control sites were highlighted also for erected algae (DvsC P b 0.0147) and foraminifers (DvsC P b 0.0096), with mean higher values in Disturbed site compared with Control ones, especially from 2013 onwards
(Fig. 5). Only PERMDISP results obtained for foraminifers cover indicated a significant dispersion among samples (P b 0.001). No significant differences between Disturbed and Control sites occurred for hydroids, bryozoans, spirorbids and ascidians cover. Moreover, there was no evidence of differences between the two Control sites for any of the taxa considered (Fig. 5). The analysis detected significant higher values for broken tips in Disturbed site than in the Control sites (TixDvsC P b 0.03), especially in July 2013 and July 2014, while no significant evidence of differences occurred for leaf surface and brown senescence tissue length between sites. Similarly, there were no differences between the two Control sites for any of these biotic variables (Fig. 6). 4. Discussion
Fig. 4. Mean (±s.e.) percentage cover of total algae and total animals in Disturbed (D) and Control (C1 and C2) sites (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; ***P b 0.001).
Effects of Costa Concordia event on P. oceanica canopy were detected. Evidence of differences on epiphytic assemblages and some biotic features of leaves was found between Control sites and Disturbed site, where disturbance signals on macrostructure of the meadow were also identified (personal observation). Conversely, epiphytic assemblages and canopy biotic traits remained unchanged between the Control sites throughout the whole study period, confirming a correct selection of the reference sites for this case of study. With regard to the epiphytic community of P. oceanica leaves, the analysis carried out on the macroalgal assemblages highlighted that crustose coralline algae was the group of algae most threatened by the wreck of Costa Concordia, at least in the first period after the naval disaster. These organisms, belonging to the genera Hydrolithon (Foslie) Foslie, 1909 and Pneophyllum Kutzing, 1843, generally dominated and characterized most of the leaf surfaces, according to the oligotrophic characteristics of water column investigated, where the epiphytic assemblage is generally dominated by crustose coralline algae (Keuskamp, 2004). Decrease of coralline algae in our data mirrored
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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Fig. 5. Mean (±s.e.) percentage cover of each epiphyte group in Disturbed (D) and Control sites (C1 and C2) (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; **P b 0.01).
other results (Balata et al., 2007; Martínez-Crego et al., 2010) in a moderately disturbed P. oceanica meadow. However, lack of differences between Disturbed and Control sites from March 2013 onwards highlights temporary effects on these species and a fast recovery of these encrusting assemblages. Differently, higher cover of erected macroalgae was detected near the wreck, mainly represented by brown algae of the epiphytic
association Myrionemo-Giraudietum sphacelarioidis Van der Ben 1971, which generally typify an epiphytic community in its mature stage (Casola et al., 1987). Our findings show effects on erected macroalgae, especially from July 2013 onwards, when the presence of the wreck together with the yard and related activities have completely changed the natural characteristics of the original site, suggesting the occurrence of disturbances in continuous evolution. In this regard, in fact, brown
Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012
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T. Bacci et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx
Fig. 6. Mean (±s.e.) of selected biometric features in Disturbed (D) and Control sites (C1 and C2) (July 2012, March 2013, July 2013, March 2014, July 2014). Significant differences between Disturbed and Control sites are shown (*P b 0.05; **P b 0.01; ***P b 0.001).
algae have been shown to be favored with respect to the other functional components of the epiphyte community in condition of a moderate nutrient increase because of their faster-growing ecology (Lepoint et al., 2007). With regard to the faunal assemblages, the increase of foraminifers abundance on P. oceanica leaves, as well as the increase of their variance in the site near the wreck from March 2013 onwards, does not seem to find an easy explanation since no similar evidence in the literature is known. Epiphytic foraminiferal populations usually respond to nutrient enrichment with a decrease in abundance, thus they may be useful indicators of ecosystem decline in subtropical–tropical, oligotrophic marine habitats (Richardson, 2006). Although these protozoans in surface sediments colonized by P. oceanica have been shown to be useful indicators to characterize a given environment in an integrated way (MateuVicens et al., 2014), no information is reported about the possible significant changes of foraminifers in leaf epiphytic assemblages colonizing disturbed meadows of P. oceanica (Piazzi et al., 2015). Therefore, further investigations should be carried out on the use of this taxon as bioindicator in epiphytic community studies on P. oceanica. However, changes in foraminifers abundance, as well as differences in their patterns of distribution and each other difference between
Disturbed and Control sites may have been due to other source of disturbance existing in the site near the wreck. In fact, Costa Concordia wreck acted as an artificial reef, forming a large additional submerged solid substrate (about 10,000 m2) subjected to fouling attack. Settlement and growth of marine plants and animals on the wreck may have interacted with the epiphytic community of the neighboring meadow. In this regard, distance from rocky reefs has been shown to have a direct influence on the structure of adjacent epiphytic assemblages (Van Elven et al., 2004). In addition, water motion which probably occurred near the wreck has been shown to be an important parameter in the epiphytes colonization (Fresi et al., 1982; Kendrick and Burt, 1997), especially where water turbulence can affect the availability of potential preys such as zooplankton and particulate matter for suspension feeders (McKinney and Jackson, 1989; Wahl, 1989). The level of confinement in the Disturbed site, which was changed through time firstly with the sinking of the ship and secondly with construction of the yard for the ship removal, may have had a bearing on local hydrodynamics, promoting partly the tip erosion of the canopy, especially in the summertime in the more advanced period of the study. In addition, although no significant differences occurred for senescence tissue length, a higher mean value in the Disturbed site than in the Control sites occurred in July 2012 representing a stress marker of the meadow near the wreck. The different confinement of the Disturbed site due to the presence of the wreck, and the effects of snatchy spills just after the Costa Concordia accident, or a combined effect of both, could justify the enhanced tip senescence in the summer, when the leaf growth was in its mature stage, and the plant still was not accustomed to the new conditions. In conclusion, our results show effects of Costa Concordia event both on epiphytic assemblages and biotic features of P. oceanica canopy, suggesting however a reduced influence of the chemical pollution, as also confirmed by results of studies carried out on biomarkers Mytilus galloprovincialis in the same study area (Regoli et al., 2014). According to these results, serious contamination events or consistent increase of environmental pollution should be excluded as only some episodic spills with reversible effects emerged (Regoli et al., 2014). Moreover, structure of the canopy and its epiphytic assemblages could have been affected by synergic effects among factors associated with the body of the wreck and those related to the removal yard, where the first could have acted as a physical barrier to the natural hydrodynamics of the area, changing significantly the submerged landscape of the Disturbed site. Acknowledgements The Monitoring Plan was founded by the Italian National Civil Protection Agency in the framework of the Costa Concordia accident emergency. References Alcoverro, T., Pérez, M., Romero, J., 2004. Importance of within-shoot epiphyte distribution for the carbon budget of seagrasses: the example of Posidonia oceanica. Bot. Mar. 47. http://dx.doi.org/10.1515/BOT.2004.036. Allen Price, W., Macauley, J.M., Clark, J.R., 1986. Effects of drilling fluids on Thalassia testudinum and its epiphytic algae. Environ. Exp. Bot. 26, 321–330. http://dx.doi. org/10.1016/0098-8472(86)90019-5. Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26, 32–46. http://dx.doi.org/10.1111/j.1442-9993.2001.01070.pp.x. Anderson, M.J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253. http://dx.doi.org/10.1111/j.1541-0420.2005.00440.x. Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. 2008. ARPAT, 2012. Monitoraggio della qualità ambientale nell'area interessata dall'incidente della nave Costa Concordia. Report. p. 71. Balata, D., Nesti, U., Piazzi, L., Cinelli, F., 2007. Patterns of spatial variability of seagrass epiphytes in the north-west Mediterranean Sea. Mar. Biol. 151, 2025–2035. http://dx. doi.org/10.1007/s00227-006-0559-y.
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Please cite this article as: Bacci, T., et al., Effects of Costa Concordia shipwreck on epiphytic assemblages and biotic features of Posidonia oceanica canopy, Marine Pollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.06.012