- Email: [email protected]
Reply to “Letter to the editor regarding the article ‘Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods’ by Alagna et al., published in Marine Pollution Bulletin, 149: 2019 (110578)” by Calvo et al. Marine Pollution Bulletin, 158:2020 (111395)
Marine Pollution Bulletin 161 (2020) 111754
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Correspondence Reply to “Letter to the editor regarding the article ‘Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods’ by Alagna et al., published in Marine Pollution Bulletin, 149: 2019 (110578)” by Calvo et al. Marine Pollution Bulletin, 158:2020 (111395)
T
ARTICLE INFO
ABSTRACT
Keywords: Restoration Substrate Habitat Ecological engineering Posidonia oceanica
Calvo et al. (2020) criticize a new seagrass rehabilitation method proposed by Alagna et al. (2019) and inspired by the Posidonia oceanica spontaneous recovery observed at Capo Feto (Sicily), were recolonization was detected almost exclusively on rubbles deployed to fill a pipeline trench. Calvo et al. (2020) claim that natural recovery occurred consistently also on dead matte along the eastern side of the trench, weakening the assumption on which the method is based. Here we show that the P. oceanica patches reported by these authors as new es tablishments were already documented in 2003 (Vega Fernandez et al., 2005) and are attributable to the fragmentation of the pristine meadow caused by altered sedimentation rate after an extensive dredging op eration. Moreover, we outline the area of applicability of the method tested in Alagna et al. (2019) and provide a point-by-point rebuttal to the complaints of imprecise and misleading contents of the paper.
1. Introduction On reading the letter to the Editor of Marine Pollution Bulletin by Calvo et al. (2020), our first thought was: Goodness! Perhaps the Po sidonia oceanica recolonization on rubble mounds, observed and docu mented in our previous articles on Capo Feto (see Box 1), was not as persistent as we thought and the recolonizing patches were destroyed by a storm. Further examination, however, revealed that this letter regarded something different and for the most part not directly related to the Alagna et al. (2019) paper but rather to that by Badalamenti et al. (2011), which reported ROV observations made between 1993 and 99. According to our friends at the University of Palermo, the P. oceanica meadow at Capo Feto, which was damaged twice by dredging activities in the recent past (1987/88 and 1992/93), seemed to have recovered consistently also on dead matte, and not only almost exclusively on rubble mounds, as we had previously shown (Di Carlo et al., 2005, 2007; Badalamenti et al., 2011). To support their idea, Calvo et al. (2020) show pictures of circular patches of P. oceanica surrounded by dead matte partially covered by sand. Calvo et al. (2020) claim that these circular patches, presumably of a diameter of up to a few meters, originated from seedlings that settled on the dead matte and in an unspecified timescale began colonization, forming the circular patches. Having seen the images of the P. oceanica patches provided by Calvo et al. (2020) and taken note of their location close to the eastern side of the trench at Capo Feto, we can state the following: similar patches of P. oceanica were already present after the second trench excavations of 1993 in exactly the same place reported by Calvo et al. (2020), as documented by Vega Fernández et al. (2005). The latter authors at tributed the presence of circular P. oceanica patches to a process of fragmentation of the original meadow. This fragmentation was due to the secondary impact of large amounts of sediment and coarse debris https://doi.org/10.1016/j.marpolbul.2020.111754 Received 7 October 2020; Accepted 7 October 2020 Available online 27 October 2020 0025-326X/ © 2020 Published by Elsevier Ltd.
released by the excavation and subsequent re-suspension affecting the area nearby, which resulted in the suffocation of the lower portions of the meadow (Badalamenti et al., 2006; Di Carlo et al., 2011). We argue here that the P. oceanica patches observed by Calvo et al. (2020) on the dead matte in the eastern side of the trench dug at Capo Feto between 1992 and 1993 are not the result of a colonization process by P. oceanica seedlings or vegetative propagules. Rather, they are the result, still evident today, of the fragmentation process that the meadow underwent following the excavation. In their letter, Calvo et al. (2020) also criticized the restoration method tested by Alagna et al. (2019). Here, we provide a rebuttal to these objections as well as to the claims that our paper was imprecise and misleading (Calvo et al., 2020). Moreover, we define the area of applicability of the method tested in Alagna et al. (2019) in view of the increasing need for coastal defence and climate change mitigation. 2. Posidonia oceanica patches on dead matte: sign of recovery or meadow fragmentation? One of the main criticisms by Calvo et al. (2020) of the restoration technique proposed and tested by Alagna et al. (2019) was that the assumption on which the methodology is based, i.e. that natural re covery of P. oceanica meadow occurred mainly on artificial rubble in the Capo Feto trench, is wrong. These authors claim that P. oceanica natural recovery occurred consistently also on P. oceanica dead matte. Here we provide data and documents showing that the field observa tions by Calvo et al. (2020) were, most likely, misinterpreted. Calvo et al. (2020) describe circular patches of P. oceanica on dead matte ranging in diameter from tens of cm up to 2.5 m. Patches were observed during the operations of a P. oceanica reforestation project on the eastern side of the Capo Feto trench (Calvo et al., 2020; Fig. 1). Calvo et al. (2020) state “Indeed, an evident process of spontaneous re-
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Box 1 Summary of the Capo Feto case-study. The deployment of the TRANSMED pipeline between Cape Bon (NE Tunisia) and Capo Feto (SW Sicily, Italy) entailed the dredging of two trenches through the pristine Posidonia oceanica meadow which spreads off the Capo Feto coast. The first excavation, 1980–81, caused the loss of more than 50 ha of the meadow between 0 and 30 m depth (Badalamenti et al., 2011). The trench was backfilled with residual materials from the excavation and calcarenitic boulders. The second excavation occurred in 1992–93 and consolidated calcareous rubble was used to cover the trench and stabilize the seafloor. Direct impacts to the meadow were caused by the plant removal and burial. Indirect impacts followed due to sediment plume, sediment movement and altered sedimentation regime which caused an overall loss of 81.20 ha of the pristine P. oceanica bed (Badalamenti et al., 2011). In 1993 the area exhibited a mosaic of heterogeneous substrates, including sand, gravel, calcarenitic boulders, dead matte and quarry rocks, on which spontaneous recovery of P. oceanica through vegetative fragments was documented from 1993 to 1999 (Badalamenti et al., 2011). Results showed that substantial recovery of P. oceanica occurred only on artificial mounds made of the quarry calcareous rubble used to backfill the trench after the second excavation, with an overall estimation of 3.24 ha of seagrass cover gained after seven years, while on the other substrates P. oceanica cover did not exceed 2% (Badalamenti et al., 2011). A survey conducted in 2010 documented that recolonizing patches on rubble persisted, developed and began to merge, producing a small meadow (Badalamenti et al., 2010, Fig. 4). Badalamenti et al. (2011) suggested that the successful recolonization observed at the Capo Feto trench was facilitated by the great availability of vegetative fragments detached from the surrounding meadow acting as recolonizing units, and by the specific features of the rubble field, which provided proper stability and topographical complexity at the adequate scale for the propagules to settle (cm - tens of cm). These features allowed vegetative fragments to embed themselves between rock crevices on several occasions and to persist even in high energy conditions, favouring establishment and recruitment over time. Starting from the observation of P. oceanica natural recolonization patterns, Alagna et al. (2019) tested an innovative transplantation method in order to identify those habitat features conducive to successful propagule establishment. The ecological knowledge previously acquired was used to develop and test an alternative approach to restoration, taking inspiration from the strong recovery potential exhibited by P. oceanica in the Capo Feto pipeline trench. In order to mimic the spontaneous recolonization of P. oceanica vegetative fragments observed on the rubble field, gabions filled with calcareous rocks of selected sizes were used as transplanting substrate units on which P. oceanica cuttings were secured with different anchoring devices (Alagna et al., 2019). The restoration method exhibited very high transplant survival after thirty months (from 88.89 ± 3.93% to 54.17 ± 6.16%, depending on the anchoring devices) despite the strong hydrodynamic regime and the disturbance from fishing gears operating in the study area. Moreover, transplant branching meant the initial planting density was exceeded, with an overall shoot survival of 274.72% to 422.22% after thirty months (Alagna et al., 2019).
colonization of P. oceanica on dead matte is occurring, since natural circular patches of different sizes can be recognized (Fig. 1). This finding is missing in Alagna et al. (2019) probably because the structure of the aforementioned survey was not sufficiently extensive in space and/or in time to capture the full variability of P. oceanica recruitment on the different substrates present [page 2, point 2]”. As previously mentioned, Calvo et al. (2020), attributed to the paper by Alagna et al. (2019) the aims and the results reported by Badalamenti et al. (2011). Consequentely, Calvo et al. (2020) compared their observations, made in 2019, not with data within Alagna et al. (2019) but with data re corded 20 years earlier by Badalamenti et al. (2011) during a survey that, we reckon, was sufficiently extensive in space and time to capture the full variability of P. oceanica recruitment on the different substrates present at that time. However, this finding by Calvo et al. (2020) is based solely on observations. They provide no evidence to attribute these patches to new establishment by sexual or vegetative propagules, rather than to residual cover of the pristine meadow on the dead matte near the trench border. In our opinion, the “process of spontaneous re-colonization” is not “evident” since the reported pattern cannot be unambiguously ascribed to the alleged mechanism of seedling and/or vegetative fragment es tablishment and expansion. On the contrary, data and documents exist to support the hypothesis that the P. oceanica patches observed are the result of pristine meadow regression and fragmentation near the eastern trench border. In a previous study by Vega Fernández et al. (2005), the Capo Feto P. oceanica fragmentation was described when evaluating the effects of habitat fragmentation on the structure of the associated fish assem blage. These authors worked on the eastern side of the trench between 5 and 15 m depth, screening an area of about 1000 by 350 m (Fig. 1). Notably, this is the same area where the reforestation pilot plants cited by Calvo et al. (2020) (https://bluegrowth-place.eu/?p=1168) were located. Vega Fernández et al. (2005) found small circular patches of P. oceanica (of 0.5 to 1.5 m) close to the trench. Patches were separated by wide (3 to 6 m) channels of dead matte partially covered by sand. The authors referred to such patches as “highly fragmented meadow” (Fig. 2). Moving eastward (i.e. away from the trench), the meadow structure changed gradually up to the point in which a reversed land scape occurred: seagrass patches ranged between 3 and 6 m in dia meter, while channels were narrower, 0.5 to 1.5 m wide. The authors described such patches as “lowly fragmented meadow” (Fig. 2). Moving further eastward, the patches became even wider and the sandy
channels narrower, up to the “continuous meadow”, which started at about 250 m from the trench (Fig. 2). The correctness of the spatial replication by Vega Fernández et al. (2005) is supported by the consistency of the findings of the meadow fragmentation gradient from the eastern side of the trench to the con tinuous meadow at different depths. The spatial pattern persisted until the last observation made in 2003 (Vega Fernández et al., 2005). While it can be argued that the associated fish assemblage can change in a relatively short time period, it is hardly the case for seagrass patches. Indeed, the aforementioned “evident process of spontaneous [seagrass] re-colonization” reported by Calvo et al. (2020) is at odds with the findings of Vega Fernández et al. (2005). Should the process invoked be at work, one would expect to find seagrass patches of different ages and sizes interspersed in a sandy matrix of variable width. The fragmentation pattern described by Vega Fernández et al. (2005) reflects a process analogous to the one documented by Marbà and Duarte (1995) for Cymodocea nodosa in a coastal lagoon. These last authors observed that, under rough weather conditions, submarine dunes of sand moved, thereby suffocating some portions of a C. nodosa meadow. Hence, our underlying assumption is that a similar suffocation process occurred in the area close to the Capo Feto trench following the pipeline deployment. The large quantity of sediment available in the area (Badalamenti et al., 2006; Di Carlo et al., 2011) and the dominant current flowing eastward parallel to the coast for most of the year (Menna et al., 2019) generated a gradient of suffocation by sediment deposition that showed its maximum intensity near the trench border and declined eastward at increasing distance from the trench. This gradient can explain the distribution and size of the seagrass patches, which displayed a similar size range at a given distance from the trench across different depth ranges. Such a pattern of size distribution cannot be explained by the natural re-colonization process invoked by Calvo et al. (2020), since this logically predicts a homogeneous mixture of seagrass patches of different ages and sizes, generated by seedlings and/ or vegetative fragments settled at different moments over time fol lowing the dredging of 1992–1993. A further element that refutes the hypothesis of new establishment by seedlings (or by vegetative fragments) of the patches observed by Calvo et al. (2020) is their size. Sintes et al. (2006) estimated that a young clone of P. oceanica expands at a rate of 3.9 to 6.2 cm yr−1 during the first 30 years, with a mean value of about 4.8 cm yr−1. The same authors showed that a patch of about 1.4 m length would need between 35 and 60 years to develop, and would exhibit very low shoot 2
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 1. Satellite image from Google Earth of the Capo Feto trench in which the relative position of the transplantation sites by Calvo et al., 2020 and of the area investigated by Vega Fernández et al. (2005) is reported. The reforestation pilot plants by Calvo et al. (2020) are represented as red triangles. CF1, coarse sand covering rubble mounds; CF2, rubbles; CF3, dead matte. Site depth: 7–10 m (available at https://bluegrowth-place.eu/?p=1168). The area investigated in the study by Vega Fernández et al. (2005) is highlighted as a pink polygon. It extended from the upper P. oceanica limit down to 20 m depth (about 1000 m long) and from the eastern boundary of the trench to the continuous meadow (about 350 m wide). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
density during the first 70 to 120 years of life (Sintes et al., 2006). Patch development by seedlings can be even slower (Balestri et al., 2017). Very few studies estimate the rhizome growth rate of P. oceanica seedlings (Balestri et al., 1998; Piazzi et al., 1999; Alagna et al., 2013; Balestri et al., 2017). Elongation of a seedling rhizome can range from 0.84 cm yr−1 (Balestri et al., 1998) to 2.5 cm yr−1 (Alagna et al., 2013). However, the only study that has followed patch development by seedlings over time documented an expansion of only 10 cm in 11 years (Balestri et al., 2017). Thus, even supposing that a seedling settled in 1994, immediately after the last dredging event in the study area (26 years ago, not 40, because the second dredging profoundly altered the substrate in the eastern side of the trench), and taking into account the maximum value reported for seedling rhizome elongation of 2.5 cm yr−1, newly es tablished patches by seedlings could barely exceed 60 cm diameter. The size of most of the patches shown in Fig. 1 by Calvo et al. (2020) is clearly too large to be compatible with the hypothesis of new estab lishment by seedlings (or by vegetative fragments) (Balestri et al., 2017; Sintes et al., 2006). The P. oceanica meadow in Western Sicily is one of the largest in the Mediterranean Sea (Telesca et al., 2015). Here, the plant flowers and produces fruits almost every year. In July 2019, there was a prodigious production of seeds from the P. oceanica meadows surrounding the study area (Fig. 3). It is no wonder that Calvo et al. (2020) observed P. oceanica seedlings on the dead matte (where they are particularly visible) in the Capo Feto area in subsequent months. However, seedling settlement and seedling recruitment followed by patch formation are different processes: the presence of the first does not imply the occur rence of the second. It is worth mentioning that while successful es tablishment of seedlings on dead matte has been widely reported in the literature (Balestri et al., 1998; Piazzi et al., 1999; Terrados et al.,
2013), according to Pereda-Briones et al. (2020), “P. oceanica seedlings are rather specific in their environmental requirements during their first 18 months of life, when their development and survival are fa voured in microsites of consolidated substratum (solid rock, and to a lesser extent P. oceanica matte)”. Overall, the circular patches of P. oceanica described by Calvo et al. (2020) are very similar in shape, size and location to those documented in what was called “highly fragmented bed” by Vega Fernández et al. (2005). In our opinion, which is supported by data, these formations are attributable to a process of fragmentation of the pristine meadow due to the secondary impact of the very large amount of sediment and coarse debris released by excavation operations and by subsequent resuspen sion in the nearby area (Badalamenti et al., 2006; Di Carlo et al., 2011). 3. The Posidonia oceanica matte In their letter, Calvo et al. (2020) stated that in Sicilian waters “about 54% of meadows settle on matte, 24% on sand and 20% on rocky bottom…” (Calvo et al., 2010). Were this statement correct, one would argue that a large portion of the Sicilian P. oceanica meadows died at a certain point and then recovered via propagule settlement, followed by recruitment and establishment, on the dead P. oceanica matte. The matte is not a primary substrate where a propagule can “settle”. According to Kendrick et al. (2005) “P. oceanica rhizomes de velop a complex network, known as the matte”. So, the matte is a sec ondary substrate formed primarily by P. oceanica rhizomes and is part of the plant structure. A dead P. oceanica matte can indeed be colonized by the plant via propagule settlement and establishment. Stating that 54% of P. oceanica in Sicily “settle on matte” means that it has settled on dead matte. Rather, it would be more correct to state that 54% of the Sicilian P. oceanica grows forming matte, which is a completely 3
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 2. Gradient of meadow fragmentation along the eastern trench boundary documented in Vega Fernández et al. (2005) at depth ranging from 5 to 15 m. Modified from Vega Fernández et al. (2005). Pictures were taken in 1998.
different statement. The real question is where, on which substrate, did P. oceanica settle and become established at the very beginning of co lonization? This question should be asked also for P. oceanica growing on sand. Did P. oceanica settle and become established directly on sand? Or did the sand arrive successively and the establishment occurred on a consolidated substrate? Data from Capo Feto show that natural rhizome settlement may occur much more frequently on a consolidated rocky substrate than on the other substrates available. Similar results have been reported by other authors for P. oceanica seedlings (Alagna et al., 2013; Alagna et al., 2015; Badalamenti et al., 2015; Balestri et al., 2017;
Pereda-Briones et al., 2020). We have no information on documented natural settlement, recruitment and establishment of P. oceanica vege tative fragments on sandy bottoms. At Capo Feto, P. oceanica lies on a rocky platform, and has formed matte at shallow and intermediate depths. The dead matte found close to the eastern side of the trench is the result of the impact of burial by sediment on the living meadow. Inside the trench area, the excavation made by a dredge determined the removal of both the living plant, the matte underneath and the primary rocky substrate on which the plant became established many years before. Hence, in similar areas
Fig. 3. Massive production and beach wracking of Posidonia oceanica fruits and seeds along the western coast of Sicily (Italy) in the early summer of 2019. 4
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 4. Posidonia oceanica patches originated by spontaneous recolonization on rubble in the Cape Feto trench. Left picture: the vertical section of a patch after removing rubble by hand, showing a developing matte. Pictures were taken in 2010.
impacted by dredging, there is no presence of “dead matte” but of a secondary substrate deployed by humans. The idea proposed by Alagna et al. (2019), derived from observation of the self-recruitment and es tablishment of P. oceanica on rubble mounds, was and still is aimed at restoring severely damaged areas where no sign of P. oceanica remains (including the dead matte) because of dredging or severe sediment burial. Therefore, we refute the disagreement by Calvo et al. (2020) that “… restoring the original features of the habitat where the seagrass originally established itself by mimicking the primary rocky substrate …” is a valuable choice under the circumstances described above.
The technique developed and tested by Alagna et al. (2019) is ad dressed to those cases in which the marine environment has already been markedly altered by human interventions. Indeed, it is not in tended for small, natural patches of sand or dead matte interspersed within seagrass meadows, as suggested by Calvo et al. (2020). Our technique is meant to be employed when coastal engineering, such as pipeline and cable deployment involving dredging and back filling of the seafloor, have caused the direct removal of seagrass meadows or their severe burial. These kinds of physical impacts are usually restricted in time and entail the destruction of above- and be lowground plant organs, with the replacement of the primary settle ment substrate by allochthonous ones. In other circumstances, long-term wastewater discharge by urban and industrial settlements and illegal dumping of waste materials have led to the loss of seagrass meadows along the coast, due to direct pro gressive burial and indirect impact of habitat quality degradation. Also in these cases, the primary substrate on which the meadow settled is replaced by a secondary one, often composed of unconsolidated sandy and muddy sediments. In all these cases, the introduction of a small layer of rocky substrate both as free rubble bed or caged in gabion mattresses can be employed to stabilize the seafloor and facilitate initial transplant establishment. The rationale for the introduction of a hard substrate on the seafloor is the following: where the causes of meadow regression have been removed and habitat quality reinstated, a negative outcome of seagrass restoration is due mostly to failure of the anchorage system employed to support propagule establishment during the first years after transplan tation (Meinesz et al., 1993; Molenaar and Meinesz, 1995; Vangeluwe, 2007). In other words, substrate instability at transplantation sites re presents the main feature hampering propagule recruitment, and a certain degree of stabilization of the seafloor is needed, especially for those species growing in rough waters or at exposed restoration sites. Reconstructed rocky substrates such as loose rubble beds, engineered rocky reefs and gabion mattresses provide a stable settlement for sea grass propagules, which, if appropriately dimensioned, do not move even when subject to strong currents and waves. Gaps between rocks ensure topographical complexity at the same scale of the propagules, into which cuttings, rhizomes and even seedlings can be inserted, using different anchoring supports if necessary (Alagna et al., 2019; Alagna et al., 2020). Rock size must be scaled to the hydrodynamic condition of the restoration site, to ensure stability, and to the propagule type chosen for restoration in order to obtain optimal topographical com plexity. Moreover, the height of the rocky layer can be adjusted to counteract sediment accretion at locations where excessive sedi mentation could bury leaf meristems before the transplanted rhizomes achieve sufficient vertical elongation. This approach to restoration allows exploitation of the documented potential of P. oceanica to recolonize through vegetative fragments that
4. Transplantation methods must be tailored to the features of the restoration site In order to better address efforts towards seagrass rehabilitation, a set of good practices is available to guide restoration actions (Calumpong and Fonseca, 2001; Boudouresque et al., 2012). It is well known that priority must be given to the protection and conservation of existing beds as well as to the natural recovery potential of species when compared to active transplantation (Orth et al., 2006; Cunha et al., 2012; Elliott et al., 2007). When a transplantation action is to be carried out, the site chosen must have hosted the target species in the past, the causes of meadow regression must have been identified and must have ceased. Moreover, the transplantation intervention should be preceded by a small-scale trial followed by at least 3 years of scientific monitoring (Boudouresque et al., 2012). There is agreement among the scientific community that the choice of the restoration technique must be not only species-specific but also site-specific, carefully taking into account current and past features as well as the history of the trans plantation location (Fonseca et al., 1998; Boudouresque et al., 2012). Accordingly, there is no unique, ideal transplantation technique con ducive to successful meadow recovery in every condition. We agree with Calvo et al., 2020 that when areas of dead matte are available, they can be prioritized for small transplantation actions, providing that: (i) the cause of seagrass regression has been identified and removed and (ii) the transplantation method applied has been successfully tested in pilot experiments (Cunha et al., 2012; Boudouresque et al., 2012). Dead matte has proved itself to be a sec ondary substrate suitable for transplantation of cuttings and seedlings (Pirrotta et al., 2015; Balestri et al., 1998), as it offers fairly stable settlement for placing anchoring devices compared to unconsolidated, mobile substrates. Dead matte has a complexity that can favour seedling retention and establishment, even in the absence of anchoring supports (Terrados et al., 2013; Pereda-Briones et al., 2018). However, there are several situations in which dead matte is not available, and the loca tions selected for restoration are characterized by other types of sub strate. In such conditions, different approaches to seagrass rehabilita tion are required. 5
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
spontaneously detach from the meadow and entangle in crevices be tween rocks (Di Carlo et al., 2005; Badalamenti et al., 2011). If in the area surrounding the restoration site P. oceanica beds are still present, they can act as a source of propagules. Alternatively, seagrass propa gules can be inserted within the rocky matrix and secured to it using different techniques. One of these techniques consists of using re vegetated, ad-hoc constructed gabion mattresses that exhibited excep tional survival and propagule development in a recent trial (Alagna et al., 2019). Indeed, the introduction of foreign materials to the sea bottom re presents a significant intervention. It entails habitat modification and must be considered with caution. Notwithstanding this, evaluation of the potential consequences of the introducing foreign materials should be weighed against the degree of human disturbance and alteration already suffered by habitats and communities at the restoration site. Further studies are needed to quantify ecosystem functions and services provided by revegetated rocky mattresses. However, initial observa tions suggest a net gain in ecological benefit when shifting from im pacted soft sediment to an introduced rocky substrate that acts as a settlement site not only for seagrass propagules but also for organisms belonging to hard bottom communities (Merces Project, Restoration of Marine, shallow soft bottoms habitats, http://www.merces-project.eu/ ). The positioning of hard substrates (both natural and artificial) in the marine environment to allow recovery of hard bottom communities or to stabilize the seafloor, aiding initial propagule establishment, is not new in restoration ecology. It has been employed for restoration of coral reefs (Fox et al., 2019; Ng et al., 2017), canopy-forming algae (Verdura et al., 2018), oyster beds (Frederick et al., 2016; Walles et al., 2016), rocky intertidal seagrasses (Park and Lee, 2010), and to facilitate initial establishment of Zostera marina shoots on sandy or muddy sub strates (van Katwijk and Hermus, 2000; Lee and Park, 2008). The use of gabion mattresses and/or of reconstructed rocky beds for seagrass replanting can find application in the context of ecological engineering (Temmerman et al., 2013; Morris et al., 2018). Soft and hybrid ecological engineering develops solutions for coastal defence based on restoration and/or creation of coastal habitats as biogenic reefs, salt marshes, seagrasses, mangroves. These habitats act as “living shorelines” (Bilkovic et al., 2016) and can be used to replace or com plement “hard” engineering infrastructures, such as seawalls, break waters, groynes and revetments (Morris et al., 2018). Examples of incorporation into engineered coastlines of artificial or semi-natural structures which can be successfully colonized by species are the deployment of rock sills beyond which marsh vegetation is planted to stabilize or recreate marsh habitats (O'Connor et al., 2011), the use of gabions filled with oyster shells to promote oyster reef de velopment for coastal protection (Walles et al., 2016), boulders em ployed in coastal armouring to maximize the ecological benefits of colonizing species (Liversage and Chapman, 2018) and the use of pre cast blocks provided with rock pools, pits and crevices suitable for species establishment in place of traditional boulders for coastal pro tection (Firth et al., 2014). Nature-based coastal defence infrastructures have the potential to offer several additional benefits compared to conventional hard-en gineered ones. Coastal vegetated habitats, including seagrasses, are adaptive, as they are able to cope with a certain degree of sea level rise thanks to the accretion of biogenic sediments and their ability to reg ulate vertical growth. Moreover, they provide other valuable ecosystem goods and services, such as provision of habitat and food, wildlife maintenance, nutrient cycling, water filtration and carbon sequestra tion (Morris et al., 2018). Due to the ability of seagrasses to act as CO2 sinks, to adjust to sea-level rise and protect the coast from high waves and storm surges, seagrass habitat restoration and creation is now being included in eco-engineering strategies for climate change adaptation and mitigation (Duarte et al., 2013).
5. Complaint of imprecise and misleading content We reported the performance of transplantation experiments (Alagna et al., 2019) only for those studies with monitoring periods of at least two years (Meinesz et al., 1993; Molenaar and Meinesz, 1995; Piazzi et al., 1998, Calvo et al., 2014b; Vangeluwe, 2007). Results ob tained from studies with briefer monitoring periods were considered too short to be informative (Boudouresque et al., 2012). When possible, we referred to ISI Web of Science publications, although sometimes only grey literature was available (Calvo et al., 2014a, Carannante, 2011, Vangeluwe, 2007). Accordingly, we did not cite survival results by Calvo et al. (2014a) because only 19 month and 6 month monitoring respectively were available for the two transplantation trials performed using the anchoring device patented by these authors. We agree with Calvo et al. (2020) that we should have cited the work by Pirrotta et al. (2015), which includes results of 6 year mon itoring, in place of Calvo et al. (2014b). However, this last study reports on a transplantation intervention using metal grids secured to the sea bottom, and showed 31% survival of transplants after 46 months. Our work did not provide imprecise or incorrect data, as the same transplant survival values were reported in Pirrotta et al. (2015) after 4 years of monitoring. The longer study by Pirrotta et al. (2015) points out that transplant survival remained stable after the fourth year until the end of the monitoring period. Transplants that successfully established started to produce new shoots by branching at the end of the second year, allowing recovery of initial planting density in six years. Indeed, the first years after a transplantation intervention represent the most critical phase for transplant establishment. Transplants still lack a rooting system and are prone to being dragged away by hydro dynamic forces, especially during extreme winter storms or to be dis turbed from sediment bioturbation (Molenaar and Meinesz, 1995, Vangeluwe, 2017, Alagna et al., 2019). After the first years have passed, established transplants begin to take root and branch. Their coloniza tion potential depends on species-specific growth programmes (Marbà and Duarte, 1998) and is proportional to the health of the transplants. A re-afforestation action must aim at labour and coast optimization, thus maximizing transplant survival. The higher the number of transplant units that survive and establish, the more they can start to elongate and branch. We agree with Calvo et al. (2020) that even initially low transplant establishment (< 50%) can give good results with time if the remaining transplants are vital and able to actively branch (Duarte et al., 2013). In accordance with this observation all the transplantation techniques tested in Alagna et al. (2019) can be considered fully suc cessful, because transplant branching allowed to recover and exceed initial planting density within only thirty months (Alagna et al., 2019). Calvo et al. (2020) complained that we erroneously defined the anchoring device for P. oceanica transplantation tested in Calvo et al. (2014a) as “partially biodegradable”. In their letter, they cited two patented products n. 0001400800/2010 and n. 102015000081824/ 2018, stating that both devices are made of a “totally biodegradable” polymer. The anchoring support tested in Calvo et al. (2014a) must be the first one, as the second patent No. 102015000081824/2018 was deposited only in 2015 and published in 2017, and thus did not exist when the contribution by Calvo et al. (2014a) was published. Patent No. 0001400800/2010 describes an anchoring device composed of a radial structure for housing seagrass cuttings made of bioplastic mate rial and a fixing stake “made of non-galvanized ferrous material to ensure adequate resistance”, as stated in the patent filing document. The different materials composing the anchoring device were also clearly represented by the figures shown in Calvo et al. (2014a). To the best of our knowledge, when our work was in preparation only one grey literature contribution (Calvo et al., 2014a) and no scientific publica tion that evaluates the performance of P. oceanica transplantation em ploying the patented products cited by Calvo et al. (2020) existed, nor does it exist now. 6
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Calvo et al. (2020) claimed that P. oceanica rhizome transplantation on a rocky substrate had already been performed in a “previous” study, citing Tomasello et al. (2019). The publication year of Tomasello et al. (2019) is the same as that of Alagna et al. (2019), so it is hard to see how it can be defined as “previous”. Moreover, Tomasello et al. (2019) is a contribution to conference proceedings, not easy to be found.
Bilkovic, D.M., Mitchell, M., Mason, P., Duhring, K., 2016. The role of living shorelines as estuarine habitat conservation strategies. Coast. Manage. 44 (3), 161–174. Boudouresque, C.F., Bernard, G., Bonhomme, P., Charbonnel, E., Diviacco, G., Meinesz, A., Pergent, G., Pergent-Martini, C., Ruitton, S., Tunesi, L., 2012. Protection and Conservation of Posidonia oceanica Meadows. RAMOGE and RAC/SPA publisher, Tunis, pp. 1–202. Calumpong, H.P., Fonseca, M.S., 2001. Seagrass transplantation and other seagrass re storation methods. In: Short, F.T., Coles, R.G. (Eds.), Global Seagrass Research Methods. Elsevier Science, pp. 425–442 (chapter 22). Calvo, S., Tomasello, A., Di Maida, G., Pirrotta, M., Buia, M.C., Cinelli, F., Cormaci, M., Furnari, G., Giaccone, G., Luzzu, F., Mazzola, A., Orestano, C., Procaccini, G., Sarà, G., Scannavino, A., Vizzini, S., 2010. Seagrasses along the Sicilian coasts. Chem. Ecol. 26, 249–266. Calvo, S., Scannavino, A., Luzzu, F., Di Maida, G., Pirrotta, M., Orestano, C., Paredes, F., Montagnino, F.M., Tomasello, A., 2014a. Tecnica di reimpianto mediante supporto biodegradabile. In: Bacci, T., La Porta, B., Maggi, C., Nonnis, O., Paganelli, D., Rende, S.F., Polifrone, M. (Eds.), “Conservazione e gestione della naturalità negli ecosistemi marino-costieri. Il trapianto delle praterie di Posidonia oceanica”. Manuali e Linee Guida n. 106/2014. ISPRA, Roma, pp. 47–51. Calvo, S., Scannavino, A., Luzzu, F., Di Maida, G., Pirrotta, M., Orestano, C., Tomasello, A., 2014b. Recupero di fondali a matte morta nel Golfo di Palermo mediante rifor estazione con Posidonia oceanica. In: Bacci, T., La Porta, B., Maggi, C., Nonnis, O., Paganelli, D., Rende, S.F., Polifrone, M. (Eds.), “Conservazione e gestione della naturalità negli ecosistemi marino-costieri. Il trapianto delle praterie di Posidonia oceanica”. Manuali e Linee Guida n. 106/2014. ISPRA, Roma, pp. 43–46. Calvo, S., Pirrotta, M., Tomasello, A., 2020. Letter to the editor regarding the article “Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods” by Alagna et al., published in Mar. Pollut. Bull., 149: 2019 (110578). Mar. Pollut. Bull. 158, 111395. Carannante, F., 2011. Monitoraggio a lungo termine di trapianti di Posidonia oceanica suvasta scala. PhD Thesis. University of Tuscia, Viterbo. Cunha, A.H., Marbá, N.N., van Katwijk, M.M., Pickerell, C., Henriques, M., Bernard, G.M., Ferreira, A., Garcia, S., Garmendia, J.M., Manent, P., 2012. Changing paradigms in seagrass restoration. Restor. Ecol. 20, 427–430. Di Carlo, G., Badalamenti, F., Jensen, A.C., Koch, E.W., Riggio, S., 2005. Colonisation process of vegetative fragments of Posidonia oceanica (L.) Delile on rubble mounds. Mar. Biol. 147, 1261–1270. Di Carlo, G., Badalamenti, F., Terlizzi, A., 2007. Recruitment of Posidonia oceanica on rubble mounds: substratum effects on biomass partitioning and leaf morphology. Aquat. Bot. 87 (2), 97–103. Di Carlo, G., Benedetti-Cecchi, L., Badalamenti, F., 2011. Response of Posidonia oceanica growth to dredging effects of different magnitude. Mar. Ecol. Prog. Ser. 423, 39–45. Duarte, C.M., Losada, I.J., Hendriks, I.E., Mazarrasa, I., Marbà, N., 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Chang. 3, 961. Elliott, M., Burdon, D., Hemingway, K.L., Apitz, S.E., 2007. Estuarine, coastal and marine ecosystem restoration: confusing management and science–a revision of concepts. Estuar. Coast. Shelf Sci. 74, 349–366. Firth, L.B., Thompson, R.C., Bohn, K., Abbiati, M., Airoldi, L., Bouma, T.J., Bozzeda, F., Ceccherelli, V.U., Colangelo, M.A., Evans, A., Ferrario, F., Hanley, M.E., Hinz, H., Hoggart, S.P., Jackson, J.E., Moore, P., Morgan, E.H., Perkol-Finkel, S., Skov, M.W., Strain, E.M., van Belzen, J., Hawkins, S.J., 2014. Between a rock and a hard place: environmental and engineering considerations when designing coastal defence structures. Coast. Eng. 87, 122–135. Fonseca, M.S., Kenworthy, W.J., Thayer, G.W., 1998. Guidelines for the Conservation and Restoration of Seagrasses in the United States and Adjacent Waters. National Marine Fisheries Service, NOAA Coastal Ocean Program, Decision Analysis Series. Fox, H.E., Harris, J.L., Darling, E.S., Ahmadia, G.N., Razak, T.B., 2019. Rebuilding coral reefs: success (and failure) 16 years after low-cost, low-tech restoration. Restor. Ecol. 27 (4), 862–869. Frederick, P., Vitale, N., Pine, B., Seavey, J., Sturmer, L., 2016. Reversing a rapid decline in oyster reefs: effects of durable substrate on oyster populations, elevations, and aquatic bird community composition. J. Shellfish Res. 35 (2), 359–367. Kendrick, G.A., Marbà, N., Duarte, C.M., 2005. Modelling formation of complex topo graphy by the seagrass Posidonia oceanica. Estuar. Coast. Shelf Sci. 65 (4), 717–725. Lee, K.S., Park, J.I., 2008. An effective transplanting technique using shells for restoration of Zostera marina habitats. Mar. Pollut. Bull. 56 (5), 1015–1021. Liversage, K., Chapman, M.G., 2018. Coastal ecological engineering and habitat re storation: incorporating biologically diverse boulder habitat. Mar. Ecol. Prog. Ser. 593, 173–185. Marbà, N., Duarte, C.M., 1995. Coupling of seagrass (Cymodocea nodosa) patch dynamics to subaqueous dune migration. J. Ecol. 83, 381–389. Marbà, N., Duarte, C.M., 1998. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 174, 269–280. Meinesz, A., Caye, G., Loques, F., Molenaar, H., 1993. Polymorphism and development of Posidonia oceanica transplanted from different parts of the Mediterranean into the National Park of port-Cros. Bot. Mar. 36, 209–216. Menna, M., Poulain, P.M., Ciani, D., Doglioli, A., Notarstefano, G., Gerin, R., Rio, M.H., Santoleri, R., Gauci, A., Drago, A., 2019. New insights of the Sicily Channel and southern Tyrrhenian Sea variability. Water 11, 1355. Molenaar, H., Meinesz, A., 1995. Vegetative reproduction in Posidonia oceanica: survival and development of transplanted cuttings according to different spacings, arrange ments and substratum. Bot. Mar. 38, 313–322. Morris, R.L., Konlechner, T.M., Ghisalberti, M., Swearer, S.E., 2018. From grey to green: efficacy of eco-engineering solutions for nature-based coastal defence. Glob. Change Biol. 24 (5), 1827–1842.
6. Conclusions Two ecological processes, namely re-colonization and habitat frag mentation, can sometimes lead to a similar landscape. When only a snapshot of a process is available, the possibility of mistaking the actual ongoing process is very high. This is what possibly took place when Calvo et al. were shown pictures of the P. oceanica circular patches at Capo Feto by the team of Biosurvey S.r.l., an academic spin-off of the University of Palermo which performed the transplantation operations. The presence of a very large number of seedlings on the sea bottom due to the abnormally great production and release of seeds by the western Sicilian P. oceanica meadow between spring and summer 2019 very likely contributed to the erroneous conclusion that the patches ob served were the result of seedling colonization. Regarding the restoration of damaged P. oceanica beds we agree that further impacts to, and consequent loss of the existing meadows should be avoided as much as possible, if not prevented completely. We believe that knowledge of the ecology of seagrasses and of P. oceanica needs to be improved. The natural recovery of P. oceanica on rubble mounds observed for several years at Capo Feto prompted research on the co lonization process and on the possibility of restoring heavily impacted areas to conditions similar to those the species found once the coloni zation started. We still have a long way to go before we can predict the outcome of a restoration action. The Capo Feto experience has provided the chance to identify some habitat features which are conducive to successful P. oceanica meadow recovery. The presence of these features should be recommended at sites targeted for restoration actions in order to im prove the likelihood of positive transplantation outcomes. References Alagna, A., Vega Fernández, T., Terlizzi, A., Badalamenti, F., 2013. Influence of micro habitat on seedling survival and growth of the Mediterranean seagrass Posidonia oceanica (L.) Delile. Estuar. Coast. Shelf Sci. 119, 119–125. Alagna, A., Vega Fernández, T., Anna, G.D., Magliola, C., Mazzola, S., Badalamenti, F., 2015. Assessing Posidonia oceanica seedling substrate preference: an experimental determination of seedling anchorage success in rocky vs. sandy substrates. PLoS One 10 (4), e0125321. Alagna, A., D'Anna, G., Musco, L., Vega Fernández, T., Gresta, M., Pierozzi, N., Badalamenti, F., 2019. Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods. Mar. Pollut. Bull. 149, 110578. Alagna, A., Zenone, A., Badalamenti, F., 2020. The perfect microsite: how to maximize Posidonia oceanica seedling settlement success for restoration purposes using ecolo gical knowledge. Mar. Environ. Res. 161, 104846. Badalamenti, F., Di Carlo, G., D’Anna, G., Gristina, M., Toccaceli, M., 2006. Effects of dredging activities on population dynamics of Posidonia oceanica (L.) Delile in the Mediterranean Sea: the case study of capo Feto (SW Sicily, Italy). Hydrobiologia 555, 253–261. Badalamenti, F., Alagna, A., D’Anna, G., Di Stefano, G., Vega Fernández, T., 2010. Sperimentazone di metodologie di facilitazione del reclutamento di germogli di Posidonia oceanica finalizzate al ripristino delle praterie. Rapporto Tecnico, contratto n. 524645 del 26/07/2010. Consulenza scientifica nel campo del ripristino delle praterie di Posidonia oceanica per SAIPEM S.p.A. IAMC-CNR. U.O.S. di Mazara del Vallo, Sede distaccata di Castellammare del Golfo, Trapani, Italy, pp. 1–81. Badalamenti, F., Alagna, A., D’Anna, G., Terlizzi, A., Di Carlo, G., 2011. The impact of dredge-fill on Posidonia oceanica seagrass meadows: regression and patterns of re covery. Mar. Pollut. Bull. 62, 483–489. Badalamenti, F., Alagna, A., Fici, S., 2015. Evidences of adaptive traits to rocky substrates undermine paradigm of habitat preference of the Mediterranean seagrass Posidonia oceanica. Sci. Rep. 5 (1), 1–6. Balestri, E., Piazzi, L., Cinelli, F., 1998. Survival and growth of transplanted and natural seedlings of Posidonia oceanica (L.) Delile in a damaged coastal area. J. Exp. Mar. Biol. Ecol. 228 (2), 209–225. Balestri, E., Vallerini, F., Lardicci, C., 2017. Recruitment and patch establishment by seed in the seagrass Posidonia oceanica: importance and conservation implications. Front. Plant Sci. 8, 1067.
7
Marine Pollution Bulletin 161 (2020) 111754
Correspondence Ng, C.S.L., Toh, T.C., Chou, L.M., 2017. Artificial reefs as a reef restoration strategy in sediment-affected environments: insights from long-term monitoring. Aquat. Conserv. 27 (5), 976–985. O’Connor, M.I., Violin, C.R., Anton, A., Ladwig, L.M., Piehler, M.F., 2011. Salt marsh stabilization affects algal primary producers at the marsh edge. Wetl. Ecol. Manag. 19 (2), 131–140. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L., Hughes, R.A., Kendrick, G.A., Kenworthy, W.J., Olyarnik, S., Short, F.T., Waycott, M., Williams, S.L., 2006. A global crisis for seagrass ecosystems. BioScience 56, 987–996. Park, J.I., Lee, K.S., 2010. Development of transplantation method for the restoration of surfgrass, Phyllospadix japonicus, in an exposed rocky shore using an artificial un derwater structure. Ecol. Eng. 36 (4), 450–456. Pereda-Briones, L., Infantes, E., Orfila, A., Tomas, F., Terrados, J., 2018. Dispersal of seagrass propagules: interaction between hydrodynamics and substratum type. Mar. Ecol. Prog. Ser. 593, 47–59. Pereda-Briones, L., Terrados, J., Agulles, M., Tomas, F., 2020. Influence of biotic and abiotic factors of seagrass Posidonia oceanica recruitment: identifying suitable mi crosites. Mar. Environ. Res. 105076. Piazzi, L., Balestri, E., Magri, M., Cinelli, F., 1998. Experimental transplanting of Posidonia oceanica (L.) Delile into a disturbed habitat in the Mediterranean Sea. Bot. Mar. 41 (1–6), 593–602. Piazzi, L., Acunto, S., Cinelli, F., 1999. In situ survival and development of Posidonia oceanica (L.) Delile seedlings. Aquat. Bot. 63 (2), 103–112. Pirrotta, M., Tomasello, A., Scannavino, A., Di Maida, G., Luzzu, F., Bellissimo, G., Bellavia, C., Costantini, C., Orestano, C., Sclafani, G., Calvo, S., 2015. Transplantation assessment of degraded Posidonia oceanica habitats: site selection and long-term monitoring. Mediterr. Mar. Sci. 16 (3), 591–603. Sintes, T., Marbà, N., Duarte, C.M., 2006. Modeling nonlinear seagrass clonal growth: assessing the efficiency of space occupation across the seagrass flora. Estuar. Coasts 29 (1), 72–80. Telesca, L., Belluscio, A., Criscoli, A., Ardizzone, G., Apostolaki, E.T., Fraschetti, S., Gristina, M., Knittweis, L., Martin, C.S., Pergent, G., Alagna, A., Badalamenti, F., Garofalo, G., Gerakaris, V., Pace, M.L., Pergent-Martini, C., Salomidi, M., 2015. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep. 5, 12505. Temmerman, S., Meire, P., Bouma, T.J., Herman, P.M., Ysebaert, T., De Vriend, H.J., 2013. Ecosystem-based coastal defence in the face of global change. Nature 504 (7478), 79–83. Terrados, J., Marin, A., Celdrán, D., 2013. Use of Posidonia oceanica seedlings from beach-
cast fruits for seagrass planting. Bot. Mar. 56 (2), 185–195. Tomasello, A., Pirrotta, M., Calvo, S., 2019. Construction underwater landscape by using Posidonia oceanica transplanting combined with innovative artificial reefs. In: Proceedings of the 6th Mediterranean Symposium on Marine Vegetation, Antalya,Turkey, 14–18 January 2019, pp. 92–96. http://www.rac-spa.org/sites/ default/files/symposium/proceedings_msmv_2019_final.pdf. van Katwijk, M.M., Hermus, D.C.R., 2000. Effects of water dynamics on Zostera marina: transplantation experiments in the intertidal Dutch Wadden Sea. Mar. Ecol. Prog. Ser. 208, 107–118. Vangeluwe, D., 2007. Effets de la transplantation sur la biométrie et sur la dynamique des nutriments, du carbone et de la chlorophylle de Posidonia oceanica (L.) Delile. M.Sc. Thesis. University of Liège. Vega Fernández, T., Milazzo, M., Badalamenti, F., D’Anna, G., 2005. Comparison of the fish assemblage associated with Posidonia oceanica after the partial loss and con sequent fragmentation of the meadow. Estuar. Coast. Shelf Sci. 65 (4), 645–653. Verdura, J., Sales, M., Ballesteros, E., Cefalì, M.E., Cebrian, E., 2018. Restoration of a canopy-forming alga based on recruitment enhancement: methods and long-term success assessment. Front. Plant Sci. 9, 1832. Walles, B., Troost, K., van den Ende, D., Nieuwhof, S., Smaal, A.C., Ysebaert, T., 2016. From artificial structures to self-sustaining oyster reefs. J. Sea Res. 108, 1–9.
Adriana Alagnaa,b, , Giovanni D'Annaa, Luigi Muscob, Tomás Vega Fernándezb, Martina Grestac, Natalia Pierozzic, Fabio Badalamentia,b,d a CNR-IAS, Institute for the study of Anthropic Impacts and Sustainability of the Marine Environment, Via G. da Verrazzano 17, 91014 Castellammare del Golfo, TP, Italy b Stazione Zoologica Anton Dohrn, Integrative Marine Ecology Department, Villa Comunale, 80121 Naples, Italy c Saipem S.p.A., via Martiri di Cefalonia 67, 20097 San Donato Milanese, MI, Italy d School of Geosciences, Grant Institute, King's Buildings, University of Edinburgh, Edinburgh, United Kingdom E-mail address: [email protected] (A. Alagna). ⁎
⁎ Corresponding author at: CNR-IAS, Institute for the Study of Anthropic Impacts and Sustainability of the Marine Environment, Via G. da Verrazzano 17, 91014 Castellammare del Golfo, TP, Italy.
8
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Correspondence Reply to “Letter to the editor regarding the article ‘Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods’ by Alagna et al., published in Marine Pollution Bulletin, 149: 2019 (110578)” by Calvo et al. Marine Pollution Bulletin, 158:2020 (111395)
T
ARTICLE INFO
ABSTRACT
Keywords: Restoration Substrate Habitat Ecological engineering Posidonia oceanica
Calvo et al. (2020) criticize a new seagrass rehabilitation method proposed by Alagna et al. (2019) and inspired by the Posidonia oceanica spontaneous recovery observed at Capo Feto (Sicily), were recolonization was detected almost exclusively on rubbles deployed to fill a pipeline trench. Calvo et al. (2020) claim that natural recovery occurred consistently also on dead matte along the eastern side of the trench, weakening the assumption on which the method is based. Here we show that the P. oceanica patches reported by these authors as new es tablishments were already documented in 2003 (Vega Fernandez et al., 2005) and are attributable to the fragmentation of the pristine meadow caused by altered sedimentation rate after an extensive dredging op eration. Moreover, we outline the area of applicability of the method tested in Alagna et al. (2019) and provide a point-by-point rebuttal to the complaints of imprecise and misleading contents of the paper.
1. Introduction On reading the letter to the Editor of Marine Pollution Bulletin by Calvo et al. (2020), our first thought was: Goodness! Perhaps the Po sidonia oceanica recolonization on rubble mounds, observed and docu mented in our previous articles on Capo Feto (see Box 1), was not as persistent as we thought and the recolonizing patches were destroyed by a storm. Further examination, however, revealed that this letter regarded something different and for the most part not directly related to the Alagna et al. (2019) paper but rather to that by Badalamenti et al. (2011), which reported ROV observations made between 1993 and 99. According to our friends at the University of Palermo, the P. oceanica meadow at Capo Feto, which was damaged twice by dredging activities in the recent past (1987/88 and 1992/93), seemed to have recovered consistently also on dead matte, and not only almost exclusively on rubble mounds, as we had previously shown (Di Carlo et al., 2005, 2007; Badalamenti et al., 2011). To support their idea, Calvo et al. (2020) show pictures of circular patches of P. oceanica surrounded by dead matte partially covered by sand. Calvo et al. (2020) claim that these circular patches, presumably of a diameter of up to a few meters, originated from seedlings that settled on the dead matte and in an unspecified timescale began colonization, forming the circular patches. Having seen the images of the P. oceanica patches provided by Calvo et al. (2020) and taken note of their location close to the eastern side of the trench at Capo Feto, we can state the following: similar patches of P. oceanica were already present after the second trench excavations of 1993 in exactly the same place reported by Calvo et al. (2020), as documented by Vega Fernández et al. (2005). The latter authors at tributed the presence of circular P. oceanica patches to a process of fragmentation of the original meadow. This fragmentation was due to the secondary impact of large amounts of sediment and coarse debris https://doi.org/10.1016/j.marpolbul.2020.111754 Received 7 October 2020; Accepted 7 October 2020 Available online 27 October 2020 0025-326X/ © 2020 Published by Elsevier Ltd.
released by the excavation and subsequent re-suspension affecting the area nearby, which resulted in the suffocation of the lower portions of the meadow (Badalamenti et al., 2006; Di Carlo et al., 2011). We argue here that the P. oceanica patches observed by Calvo et al. (2020) on the dead matte in the eastern side of the trench dug at Capo Feto between 1992 and 1993 are not the result of a colonization process by P. oceanica seedlings or vegetative propagules. Rather, they are the result, still evident today, of the fragmentation process that the meadow underwent following the excavation. In their letter, Calvo et al. (2020) also criticized the restoration method tested by Alagna et al. (2019). Here, we provide a rebuttal to these objections as well as to the claims that our paper was imprecise and misleading (Calvo et al., 2020). Moreover, we define the area of applicability of the method tested in Alagna et al. (2019) in view of the increasing need for coastal defence and climate change mitigation. 2. Posidonia oceanica patches on dead matte: sign of recovery or meadow fragmentation? One of the main criticisms by Calvo et al. (2020) of the restoration technique proposed and tested by Alagna et al. (2019) was that the assumption on which the methodology is based, i.e. that natural re covery of P. oceanica meadow occurred mainly on artificial rubble in the Capo Feto trench, is wrong. These authors claim that P. oceanica natural recovery occurred consistently also on P. oceanica dead matte. Here we provide data and documents showing that the field observa tions by Calvo et al. (2020) were, most likely, misinterpreted. Calvo et al. (2020) describe circular patches of P. oceanica on dead matte ranging in diameter from tens of cm up to 2.5 m. Patches were observed during the operations of a P. oceanica reforestation project on the eastern side of the Capo Feto trench (Calvo et al., 2020; Fig. 1). Calvo et al. (2020) state “Indeed, an evident process of spontaneous re-
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Box 1 Summary of the Capo Feto case-study. The deployment of the TRANSMED pipeline between Cape Bon (NE Tunisia) and Capo Feto (SW Sicily, Italy) entailed the dredging of two trenches through the pristine Posidonia oceanica meadow which spreads off the Capo Feto coast. The first excavation, 1980–81, caused the loss of more than 50 ha of the meadow between 0 and 30 m depth (Badalamenti et al., 2011). The trench was backfilled with residual materials from the excavation and calcarenitic boulders. The second excavation occurred in 1992–93 and consolidated calcareous rubble was used to cover the trench and stabilize the seafloor. Direct impacts to the meadow were caused by the plant removal and burial. Indirect impacts followed due to sediment plume, sediment movement and altered sedimentation regime which caused an overall loss of 81.20 ha of the pristine P. oceanica bed (Badalamenti et al., 2011). In 1993 the area exhibited a mosaic of heterogeneous substrates, including sand, gravel, calcarenitic boulders, dead matte and quarry rocks, on which spontaneous recovery of P. oceanica through vegetative fragments was documented from 1993 to 1999 (Badalamenti et al., 2011). Results showed that substantial recovery of P. oceanica occurred only on artificial mounds made of the quarry calcareous rubble used to backfill the trench after the second excavation, with an overall estimation of 3.24 ha of seagrass cover gained after seven years, while on the other substrates P. oceanica cover did not exceed 2% (Badalamenti et al., 2011). A survey conducted in 2010 documented that recolonizing patches on rubble persisted, developed and began to merge, producing a small meadow (Badalamenti et al., 2010, Fig. 4). Badalamenti et al. (2011) suggested that the successful recolonization observed at the Capo Feto trench was facilitated by the great availability of vegetative fragments detached from the surrounding meadow acting as recolonizing units, and by the specific features of the rubble field, which provided proper stability and topographical complexity at the adequate scale for the propagules to settle (cm - tens of cm). These features allowed vegetative fragments to embed themselves between rock crevices on several occasions and to persist even in high energy conditions, favouring establishment and recruitment over time. Starting from the observation of P. oceanica natural recolonization patterns, Alagna et al. (2019) tested an innovative transplantation method in order to identify those habitat features conducive to successful propagule establishment. The ecological knowledge previously acquired was used to develop and test an alternative approach to restoration, taking inspiration from the strong recovery potential exhibited by P. oceanica in the Capo Feto pipeline trench. In order to mimic the spontaneous recolonization of P. oceanica vegetative fragments observed on the rubble field, gabions filled with calcareous rocks of selected sizes were used as transplanting substrate units on which P. oceanica cuttings were secured with different anchoring devices (Alagna et al., 2019). The restoration method exhibited very high transplant survival after thirty months (from 88.89 ± 3.93% to 54.17 ± 6.16%, depending on the anchoring devices) despite the strong hydrodynamic regime and the disturbance from fishing gears operating in the study area. Moreover, transplant branching meant the initial planting density was exceeded, with an overall shoot survival of 274.72% to 422.22% after thirty months (Alagna et al., 2019).
colonization of P. oceanica on dead matte is occurring, since natural circular patches of different sizes can be recognized (Fig. 1). This finding is missing in Alagna et al. (2019) probably because the structure of the aforementioned survey was not sufficiently extensive in space and/or in time to capture the full variability of P. oceanica recruitment on the different substrates present [page 2, point 2]”. As previously mentioned, Calvo et al. (2020), attributed to the paper by Alagna et al. (2019) the aims and the results reported by Badalamenti et al. (2011). Consequentely, Calvo et al. (2020) compared their observations, made in 2019, not with data within Alagna et al. (2019) but with data re corded 20 years earlier by Badalamenti et al. (2011) during a survey that, we reckon, was sufficiently extensive in space and time to capture the full variability of P. oceanica recruitment on the different substrates present at that time. However, this finding by Calvo et al. (2020) is based solely on observations. They provide no evidence to attribute these patches to new establishment by sexual or vegetative propagules, rather than to residual cover of the pristine meadow on the dead matte near the trench border. In our opinion, the “process of spontaneous re-colonization” is not “evident” since the reported pattern cannot be unambiguously ascribed to the alleged mechanism of seedling and/or vegetative fragment es tablishment and expansion. On the contrary, data and documents exist to support the hypothesis that the P. oceanica patches observed are the result of pristine meadow regression and fragmentation near the eastern trench border. In a previous study by Vega Fernández et al. (2005), the Capo Feto P. oceanica fragmentation was described when evaluating the effects of habitat fragmentation on the structure of the associated fish assem blage. These authors worked on the eastern side of the trench between 5 and 15 m depth, screening an area of about 1000 by 350 m (Fig. 1). Notably, this is the same area where the reforestation pilot plants cited by Calvo et al. (2020) (https://bluegrowth-place.eu/?p=1168) were located. Vega Fernández et al. (2005) found small circular patches of P. oceanica (of 0.5 to 1.5 m) close to the trench. Patches were separated by wide (3 to 6 m) channels of dead matte partially covered by sand. The authors referred to such patches as “highly fragmented meadow” (Fig. 2). Moving eastward (i.e. away from the trench), the meadow structure changed gradually up to the point in which a reversed land scape occurred: seagrass patches ranged between 3 and 6 m in dia meter, while channels were narrower, 0.5 to 1.5 m wide. The authors described such patches as “lowly fragmented meadow” (Fig. 2). Moving further eastward, the patches became even wider and the sandy
channels narrower, up to the “continuous meadow”, which started at about 250 m from the trench (Fig. 2). The correctness of the spatial replication by Vega Fernández et al. (2005) is supported by the consistency of the findings of the meadow fragmentation gradient from the eastern side of the trench to the con tinuous meadow at different depths. The spatial pattern persisted until the last observation made in 2003 (Vega Fernández et al., 2005). While it can be argued that the associated fish assemblage can change in a relatively short time period, it is hardly the case for seagrass patches. Indeed, the aforementioned “evident process of spontaneous [seagrass] re-colonization” reported by Calvo et al. (2020) is at odds with the findings of Vega Fernández et al. (2005). Should the process invoked be at work, one would expect to find seagrass patches of different ages and sizes interspersed in a sandy matrix of variable width. The fragmentation pattern described by Vega Fernández et al. (2005) reflects a process analogous to the one documented by Marbà and Duarte (1995) for Cymodocea nodosa in a coastal lagoon. These last authors observed that, under rough weather conditions, submarine dunes of sand moved, thereby suffocating some portions of a C. nodosa meadow. Hence, our underlying assumption is that a similar suffocation process occurred in the area close to the Capo Feto trench following the pipeline deployment. The large quantity of sediment available in the area (Badalamenti et al., 2006; Di Carlo et al., 2011) and the dominant current flowing eastward parallel to the coast for most of the year (Menna et al., 2019) generated a gradient of suffocation by sediment deposition that showed its maximum intensity near the trench border and declined eastward at increasing distance from the trench. This gradient can explain the distribution and size of the seagrass patches, which displayed a similar size range at a given distance from the trench across different depth ranges. Such a pattern of size distribution cannot be explained by the natural re-colonization process invoked by Calvo et al. (2020), since this logically predicts a homogeneous mixture of seagrass patches of different ages and sizes, generated by seedlings and/ or vegetative fragments settled at different moments over time fol lowing the dredging of 1992–1993. A further element that refutes the hypothesis of new establishment by seedlings (or by vegetative fragments) of the patches observed by Calvo et al. (2020) is their size. Sintes et al. (2006) estimated that a young clone of P. oceanica expands at a rate of 3.9 to 6.2 cm yr−1 during the first 30 years, with a mean value of about 4.8 cm yr−1. The same authors showed that a patch of about 1.4 m length would need between 35 and 60 years to develop, and would exhibit very low shoot 2
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 1. Satellite image from Google Earth of the Capo Feto trench in which the relative position of the transplantation sites by Calvo et al., 2020 and of the area investigated by Vega Fernández et al. (2005) is reported. The reforestation pilot plants by Calvo et al. (2020) are represented as red triangles. CF1, coarse sand covering rubble mounds; CF2, rubbles; CF3, dead matte. Site depth: 7–10 m (available at https://bluegrowth-place.eu/?p=1168). The area investigated in the study by Vega Fernández et al. (2005) is highlighted as a pink polygon. It extended from the upper P. oceanica limit down to 20 m depth (about 1000 m long) and from the eastern boundary of the trench to the continuous meadow (about 350 m wide). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
density during the first 70 to 120 years of life (Sintes et al., 2006). Patch development by seedlings can be even slower (Balestri et al., 2017). Very few studies estimate the rhizome growth rate of P. oceanica seedlings (Balestri et al., 1998; Piazzi et al., 1999; Alagna et al., 2013; Balestri et al., 2017). Elongation of a seedling rhizome can range from 0.84 cm yr−1 (Balestri et al., 1998) to 2.5 cm yr−1 (Alagna et al., 2013). However, the only study that has followed patch development by seedlings over time documented an expansion of only 10 cm in 11 years (Balestri et al., 2017). Thus, even supposing that a seedling settled in 1994, immediately after the last dredging event in the study area (26 years ago, not 40, because the second dredging profoundly altered the substrate in the eastern side of the trench), and taking into account the maximum value reported for seedling rhizome elongation of 2.5 cm yr−1, newly es tablished patches by seedlings could barely exceed 60 cm diameter. The size of most of the patches shown in Fig. 1 by Calvo et al. (2020) is clearly too large to be compatible with the hypothesis of new estab lishment by seedlings (or by vegetative fragments) (Balestri et al., 2017; Sintes et al., 2006). The P. oceanica meadow in Western Sicily is one of the largest in the Mediterranean Sea (Telesca et al., 2015). Here, the plant flowers and produces fruits almost every year. In July 2019, there was a prodigious production of seeds from the P. oceanica meadows surrounding the study area (Fig. 3). It is no wonder that Calvo et al. (2020) observed P. oceanica seedlings on the dead matte (where they are particularly visible) in the Capo Feto area in subsequent months. However, seedling settlement and seedling recruitment followed by patch formation are different processes: the presence of the first does not imply the occur rence of the second. It is worth mentioning that while successful es tablishment of seedlings on dead matte has been widely reported in the literature (Balestri et al., 1998; Piazzi et al., 1999; Terrados et al.,
2013), according to Pereda-Briones et al. (2020), “P. oceanica seedlings are rather specific in their environmental requirements during their first 18 months of life, when their development and survival are fa voured in microsites of consolidated substratum (solid rock, and to a lesser extent P. oceanica matte)”. Overall, the circular patches of P. oceanica described by Calvo et al. (2020) are very similar in shape, size and location to those documented in what was called “highly fragmented bed” by Vega Fernández et al. (2005). In our opinion, which is supported by data, these formations are attributable to a process of fragmentation of the pristine meadow due to the secondary impact of the very large amount of sediment and coarse debris released by excavation operations and by subsequent resuspen sion in the nearby area (Badalamenti et al., 2006; Di Carlo et al., 2011). 3. The Posidonia oceanica matte In their letter, Calvo et al. (2020) stated that in Sicilian waters “about 54% of meadows settle on matte, 24% on sand and 20% on rocky bottom…” (Calvo et al., 2010). Were this statement correct, one would argue that a large portion of the Sicilian P. oceanica meadows died at a certain point and then recovered via propagule settlement, followed by recruitment and establishment, on the dead P. oceanica matte. The matte is not a primary substrate where a propagule can “settle”. According to Kendrick et al. (2005) “P. oceanica rhizomes de velop a complex network, known as the matte”. So, the matte is a sec ondary substrate formed primarily by P. oceanica rhizomes and is part of the plant structure. A dead P. oceanica matte can indeed be colonized by the plant via propagule settlement and establishment. Stating that 54% of P. oceanica in Sicily “settle on matte” means that it has settled on dead matte. Rather, it would be more correct to state that 54% of the Sicilian P. oceanica grows forming matte, which is a completely 3
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 2. Gradient of meadow fragmentation along the eastern trench boundary documented in Vega Fernández et al. (2005) at depth ranging from 5 to 15 m. Modified from Vega Fernández et al. (2005). Pictures were taken in 1998.
different statement. The real question is where, on which substrate, did P. oceanica settle and become established at the very beginning of co lonization? This question should be asked also for P. oceanica growing on sand. Did P. oceanica settle and become established directly on sand? Or did the sand arrive successively and the establishment occurred on a consolidated substrate? Data from Capo Feto show that natural rhizome settlement may occur much more frequently on a consolidated rocky substrate than on the other substrates available. Similar results have been reported by other authors for P. oceanica seedlings (Alagna et al., 2013; Alagna et al., 2015; Badalamenti et al., 2015; Balestri et al., 2017;
Pereda-Briones et al., 2020). We have no information on documented natural settlement, recruitment and establishment of P. oceanica vege tative fragments on sandy bottoms. At Capo Feto, P. oceanica lies on a rocky platform, and has formed matte at shallow and intermediate depths. The dead matte found close to the eastern side of the trench is the result of the impact of burial by sediment on the living meadow. Inside the trench area, the excavation made by a dredge determined the removal of both the living plant, the matte underneath and the primary rocky substrate on which the plant became established many years before. Hence, in similar areas
Fig. 3. Massive production and beach wracking of Posidonia oceanica fruits and seeds along the western coast of Sicily (Italy) in the early summer of 2019. 4
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Fig. 4. Posidonia oceanica patches originated by spontaneous recolonization on rubble in the Cape Feto trench. Left picture: the vertical section of a patch after removing rubble by hand, showing a developing matte. Pictures were taken in 2010.
impacted by dredging, there is no presence of “dead matte” but of a secondary substrate deployed by humans. The idea proposed by Alagna et al. (2019), derived from observation of the self-recruitment and es tablishment of P. oceanica on rubble mounds, was and still is aimed at restoring severely damaged areas where no sign of P. oceanica remains (including the dead matte) because of dredging or severe sediment burial. Therefore, we refute the disagreement by Calvo et al. (2020) that “… restoring the original features of the habitat where the seagrass originally established itself by mimicking the primary rocky substrate …” is a valuable choice under the circumstances described above.
The technique developed and tested by Alagna et al. (2019) is ad dressed to those cases in which the marine environment has already been markedly altered by human interventions. Indeed, it is not in tended for small, natural patches of sand or dead matte interspersed within seagrass meadows, as suggested by Calvo et al. (2020). Our technique is meant to be employed when coastal engineering, such as pipeline and cable deployment involving dredging and back filling of the seafloor, have caused the direct removal of seagrass meadows or their severe burial. These kinds of physical impacts are usually restricted in time and entail the destruction of above- and be lowground plant organs, with the replacement of the primary settle ment substrate by allochthonous ones. In other circumstances, long-term wastewater discharge by urban and industrial settlements and illegal dumping of waste materials have led to the loss of seagrass meadows along the coast, due to direct pro gressive burial and indirect impact of habitat quality degradation. Also in these cases, the primary substrate on which the meadow settled is replaced by a secondary one, often composed of unconsolidated sandy and muddy sediments. In all these cases, the introduction of a small layer of rocky substrate both as free rubble bed or caged in gabion mattresses can be employed to stabilize the seafloor and facilitate initial transplant establishment. The rationale for the introduction of a hard substrate on the seafloor is the following: where the causes of meadow regression have been removed and habitat quality reinstated, a negative outcome of seagrass restoration is due mostly to failure of the anchorage system employed to support propagule establishment during the first years after transplan tation (Meinesz et al., 1993; Molenaar and Meinesz, 1995; Vangeluwe, 2007). In other words, substrate instability at transplantation sites re presents the main feature hampering propagule recruitment, and a certain degree of stabilization of the seafloor is needed, especially for those species growing in rough waters or at exposed restoration sites. Reconstructed rocky substrates such as loose rubble beds, engineered rocky reefs and gabion mattresses provide a stable settlement for sea grass propagules, which, if appropriately dimensioned, do not move even when subject to strong currents and waves. Gaps between rocks ensure topographical complexity at the same scale of the propagules, into which cuttings, rhizomes and even seedlings can be inserted, using different anchoring supports if necessary (Alagna et al., 2019; Alagna et al., 2020). Rock size must be scaled to the hydrodynamic condition of the restoration site, to ensure stability, and to the propagule type chosen for restoration in order to obtain optimal topographical com plexity. Moreover, the height of the rocky layer can be adjusted to counteract sediment accretion at locations where excessive sedi mentation could bury leaf meristems before the transplanted rhizomes achieve sufficient vertical elongation. This approach to restoration allows exploitation of the documented potential of P. oceanica to recolonize through vegetative fragments that
4. Transplantation methods must be tailored to the features of the restoration site In order to better address efforts towards seagrass rehabilitation, a set of good practices is available to guide restoration actions (Calumpong and Fonseca, 2001; Boudouresque et al., 2012). It is well known that priority must be given to the protection and conservation of existing beds as well as to the natural recovery potential of species when compared to active transplantation (Orth et al., 2006; Cunha et al., 2012; Elliott et al., 2007). When a transplantation action is to be carried out, the site chosen must have hosted the target species in the past, the causes of meadow regression must have been identified and must have ceased. Moreover, the transplantation intervention should be preceded by a small-scale trial followed by at least 3 years of scientific monitoring (Boudouresque et al., 2012). There is agreement among the scientific community that the choice of the restoration technique must be not only species-specific but also site-specific, carefully taking into account current and past features as well as the history of the trans plantation location (Fonseca et al., 1998; Boudouresque et al., 2012). Accordingly, there is no unique, ideal transplantation technique con ducive to successful meadow recovery in every condition. We agree with Calvo et al., 2020 that when areas of dead matte are available, they can be prioritized for small transplantation actions, providing that: (i) the cause of seagrass regression has been identified and removed and (ii) the transplantation method applied has been successfully tested in pilot experiments (Cunha et al., 2012; Boudouresque et al., 2012). Dead matte has proved itself to be a sec ondary substrate suitable for transplantation of cuttings and seedlings (Pirrotta et al., 2015; Balestri et al., 1998), as it offers fairly stable settlement for placing anchoring devices compared to unconsolidated, mobile substrates. Dead matte has a complexity that can favour seedling retention and establishment, even in the absence of anchoring supports (Terrados et al., 2013; Pereda-Briones et al., 2018). However, there are several situations in which dead matte is not available, and the loca tions selected for restoration are characterized by other types of sub strate. In such conditions, different approaches to seagrass rehabilita tion are required. 5
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
spontaneously detach from the meadow and entangle in crevices be tween rocks (Di Carlo et al., 2005; Badalamenti et al., 2011). If in the area surrounding the restoration site P. oceanica beds are still present, they can act as a source of propagules. Alternatively, seagrass propa gules can be inserted within the rocky matrix and secured to it using different techniques. One of these techniques consists of using re vegetated, ad-hoc constructed gabion mattresses that exhibited excep tional survival and propagule development in a recent trial (Alagna et al., 2019). Indeed, the introduction of foreign materials to the sea bottom re presents a significant intervention. It entails habitat modification and must be considered with caution. Notwithstanding this, evaluation of the potential consequences of the introducing foreign materials should be weighed against the degree of human disturbance and alteration already suffered by habitats and communities at the restoration site. Further studies are needed to quantify ecosystem functions and services provided by revegetated rocky mattresses. However, initial observa tions suggest a net gain in ecological benefit when shifting from im pacted soft sediment to an introduced rocky substrate that acts as a settlement site not only for seagrass propagules but also for organisms belonging to hard bottom communities (Merces Project, Restoration of Marine, shallow soft bottoms habitats, http://www.merces-project.eu/ ). The positioning of hard substrates (both natural and artificial) in the marine environment to allow recovery of hard bottom communities or to stabilize the seafloor, aiding initial propagule establishment, is not new in restoration ecology. It has been employed for restoration of coral reefs (Fox et al., 2019; Ng et al., 2017), canopy-forming algae (Verdura et al., 2018), oyster beds (Frederick et al., 2016; Walles et al., 2016), rocky intertidal seagrasses (Park and Lee, 2010), and to facilitate initial establishment of Zostera marina shoots on sandy or muddy sub strates (van Katwijk and Hermus, 2000; Lee and Park, 2008). The use of gabion mattresses and/or of reconstructed rocky beds for seagrass replanting can find application in the context of ecological engineering (Temmerman et al., 2013; Morris et al., 2018). Soft and hybrid ecological engineering develops solutions for coastal defence based on restoration and/or creation of coastal habitats as biogenic reefs, salt marshes, seagrasses, mangroves. These habitats act as “living shorelines” (Bilkovic et al., 2016) and can be used to replace or com plement “hard” engineering infrastructures, such as seawalls, break waters, groynes and revetments (Morris et al., 2018). Examples of incorporation into engineered coastlines of artificial or semi-natural structures which can be successfully colonized by species are the deployment of rock sills beyond which marsh vegetation is planted to stabilize or recreate marsh habitats (O'Connor et al., 2011), the use of gabions filled with oyster shells to promote oyster reef de velopment for coastal protection (Walles et al., 2016), boulders em ployed in coastal armouring to maximize the ecological benefits of colonizing species (Liversage and Chapman, 2018) and the use of pre cast blocks provided with rock pools, pits and crevices suitable for species establishment in place of traditional boulders for coastal pro tection (Firth et al., 2014). Nature-based coastal defence infrastructures have the potential to offer several additional benefits compared to conventional hard-en gineered ones. Coastal vegetated habitats, including seagrasses, are adaptive, as they are able to cope with a certain degree of sea level rise thanks to the accretion of biogenic sediments and their ability to reg ulate vertical growth. Moreover, they provide other valuable ecosystem goods and services, such as provision of habitat and food, wildlife maintenance, nutrient cycling, water filtration and carbon sequestra tion (Morris et al., 2018). Due to the ability of seagrasses to act as CO2 sinks, to adjust to sea-level rise and protect the coast from high waves and storm surges, seagrass habitat restoration and creation is now being included in eco-engineering strategies for climate change adaptation and mitigation (Duarte et al., 2013).
5. Complaint of imprecise and misleading content We reported the performance of transplantation experiments (Alagna et al., 2019) only for those studies with monitoring periods of at least two years (Meinesz et al., 1993; Molenaar and Meinesz, 1995; Piazzi et al., 1998, Calvo et al., 2014b; Vangeluwe, 2007). Results ob tained from studies with briefer monitoring periods were considered too short to be informative (Boudouresque et al., 2012). When possible, we referred to ISI Web of Science publications, although sometimes only grey literature was available (Calvo et al., 2014a, Carannante, 2011, Vangeluwe, 2007). Accordingly, we did not cite survival results by Calvo et al. (2014a) because only 19 month and 6 month monitoring respectively were available for the two transplantation trials performed using the anchoring device patented by these authors. We agree with Calvo et al. (2020) that we should have cited the work by Pirrotta et al. (2015), which includes results of 6 year mon itoring, in place of Calvo et al. (2014b). However, this last study reports on a transplantation intervention using metal grids secured to the sea bottom, and showed 31% survival of transplants after 46 months. Our work did not provide imprecise or incorrect data, as the same transplant survival values were reported in Pirrotta et al. (2015) after 4 years of monitoring. The longer study by Pirrotta et al. (2015) points out that transplant survival remained stable after the fourth year until the end of the monitoring period. Transplants that successfully established started to produce new shoots by branching at the end of the second year, allowing recovery of initial planting density in six years. Indeed, the first years after a transplantation intervention represent the most critical phase for transplant establishment. Transplants still lack a rooting system and are prone to being dragged away by hydro dynamic forces, especially during extreme winter storms or to be dis turbed from sediment bioturbation (Molenaar and Meinesz, 1995, Vangeluwe, 2017, Alagna et al., 2019). After the first years have passed, established transplants begin to take root and branch. Their coloniza tion potential depends on species-specific growth programmes (Marbà and Duarte, 1998) and is proportional to the health of the transplants. A re-afforestation action must aim at labour and coast optimization, thus maximizing transplant survival. The higher the number of transplant units that survive and establish, the more they can start to elongate and branch. We agree with Calvo et al. (2020) that even initially low transplant establishment (< 50%) can give good results with time if the remaining transplants are vital and able to actively branch (Duarte et al., 2013). In accordance with this observation all the transplantation techniques tested in Alagna et al. (2019) can be considered fully suc cessful, because transplant branching allowed to recover and exceed initial planting density within only thirty months (Alagna et al., 2019). Calvo et al. (2020) complained that we erroneously defined the anchoring device for P. oceanica transplantation tested in Calvo et al. (2014a) as “partially biodegradable”. In their letter, they cited two patented products n. 0001400800/2010 and n. 102015000081824/ 2018, stating that both devices are made of a “totally biodegradable” polymer. The anchoring support tested in Calvo et al. (2014a) must be the first one, as the second patent No. 102015000081824/2018 was deposited only in 2015 and published in 2017, and thus did not exist when the contribution by Calvo et al. (2014a) was published. Patent No. 0001400800/2010 describes an anchoring device composed of a radial structure for housing seagrass cuttings made of bioplastic mate rial and a fixing stake “made of non-galvanized ferrous material to ensure adequate resistance”, as stated in the patent filing document. The different materials composing the anchoring device were also clearly represented by the figures shown in Calvo et al. (2014a). To the best of our knowledge, when our work was in preparation only one grey literature contribution (Calvo et al., 2014a) and no scientific publica tion that evaluates the performance of P. oceanica transplantation em ploying the patented products cited by Calvo et al. (2020) existed, nor does it exist now. 6
Marine Pollution Bulletin 161 (2020) 111754
Correspondence
Calvo et al. (2020) claimed that P. oceanica rhizome transplantation on a rocky substrate had already been performed in a “previous” study, citing Tomasello et al. (2019). The publication year of Tomasello et al. (2019) is the same as that of Alagna et al. (2019), so it is hard to see how it can be defined as “previous”. Moreover, Tomasello et al. (2019) is a contribution to conference proceedings, not easy to be found.
Bilkovic, D.M., Mitchell, M., Mason, P., Duhring, K., 2016. The role of living shorelines as estuarine habitat conservation strategies. Coast. Manage. 44 (3), 161–174. Boudouresque, C.F., Bernard, G., Bonhomme, P., Charbonnel, E., Diviacco, G., Meinesz, A., Pergent, G., Pergent-Martini, C., Ruitton, S., Tunesi, L., 2012. Protection and Conservation of Posidonia oceanica Meadows. RAMOGE and RAC/SPA publisher, Tunis, pp. 1–202. Calumpong, H.P., Fonseca, M.S., 2001. Seagrass transplantation and other seagrass re storation methods. In: Short, F.T., Coles, R.G. (Eds.), Global Seagrass Research Methods. Elsevier Science, pp. 425–442 (chapter 22). Calvo, S., Tomasello, A., Di Maida, G., Pirrotta, M., Buia, M.C., Cinelli, F., Cormaci, M., Furnari, G., Giaccone, G., Luzzu, F., Mazzola, A., Orestano, C., Procaccini, G., Sarà, G., Scannavino, A., Vizzini, S., 2010. Seagrasses along the Sicilian coasts. Chem. Ecol. 26, 249–266. Calvo, S., Scannavino, A., Luzzu, F., Di Maida, G., Pirrotta, M., Orestano, C., Paredes, F., Montagnino, F.M., Tomasello, A., 2014a. Tecnica di reimpianto mediante supporto biodegradabile. In: Bacci, T., La Porta, B., Maggi, C., Nonnis, O., Paganelli, D., Rende, S.F., Polifrone, M. (Eds.), “Conservazione e gestione della naturalità negli ecosistemi marino-costieri. Il trapianto delle praterie di Posidonia oceanica”. Manuali e Linee Guida n. 106/2014. ISPRA, Roma, pp. 47–51. Calvo, S., Scannavino, A., Luzzu, F., Di Maida, G., Pirrotta, M., Orestano, C., Tomasello, A., 2014b. Recupero di fondali a matte morta nel Golfo di Palermo mediante rifor estazione con Posidonia oceanica. In: Bacci, T., La Porta, B., Maggi, C., Nonnis, O., Paganelli, D., Rende, S.F., Polifrone, M. (Eds.), “Conservazione e gestione della naturalità negli ecosistemi marino-costieri. Il trapianto delle praterie di Posidonia oceanica”. Manuali e Linee Guida n. 106/2014. ISPRA, Roma, pp. 43–46. Calvo, S., Pirrotta, M., Tomasello, A., 2020. Letter to the editor regarding the article “Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods” by Alagna et al., published in Mar. Pollut. Bull., 149: 2019 (110578). Mar. Pollut. Bull. 158, 111395. Carannante, F., 2011. Monitoraggio a lungo termine di trapianti di Posidonia oceanica suvasta scala. PhD Thesis. University of Tuscia, Viterbo. Cunha, A.H., Marbá, N.N., van Katwijk, M.M., Pickerell, C., Henriques, M., Bernard, G.M., Ferreira, A., Garcia, S., Garmendia, J.M., Manent, P., 2012. Changing paradigms in seagrass restoration. Restor. Ecol. 20, 427–430. Di Carlo, G., Badalamenti, F., Jensen, A.C., Koch, E.W., Riggio, S., 2005. Colonisation process of vegetative fragments of Posidonia oceanica (L.) Delile on rubble mounds. Mar. Biol. 147, 1261–1270. Di Carlo, G., Badalamenti, F., Terlizzi, A., 2007. Recruitment of Posidonia oceanica on rubble mounds: substratum effects on biomass partitioning and leaf morphology. Aquat. Bot. 87 (2), 97–103. Di Carlo, G., Benedetti-Cecchi, L., Badalamenti, F., 2011. Response of Posidonia oceanica growth to dredging effects of different magnitude. Mar. Ecol. Prog. Ser. 423, 39–45. Duarte, C.M., Losada, I.J., Hendriks, I.E., Mazarrasa, I., Marbà, N., 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nat. Clim. Chang. 3, 961. Elliott, M., Burdon, D., Hemingway, K.L., Apitz, S.E., 2007. Estuarine, coastal and marine ecosystem restoration: confusing management and science–a revision of concepts. Estuar. Coast. Shelf Sci. 74, 349–366. Firth, L.B., Thompson, R.C., Bohn, K., Abbiati, M., Airoldi, L., Bouma, T.J., Bozzeda, F., Ceccherelli, V.U., Colangelo, M.A., Evans, A., Ferrario, F., Hanley, M.E., Hinz, H., Hoggart, S.P., Jackson, J.E., Moore, P., Morgan, E.H., Perkol-Finkel, S., Skov, M.W., Strain, E.M., van Belzen, J., Hawkins, S.J., 2014. Between a rock and a hard place: environmental and engineering considerations when designing coastal defence structures. Coast. Eng. 87, 122–135. Fonseca, M.S., Kenworthy, W.J., Thayer, G.W., 1998. Guidelines for the Conservation and Restoration of Seagrasses in the United States and Adjacent Waters. National Marine Fisheries Service, NOAA Coastal Ocean Program, Decision Analysis Series. Fox, H.E., Harris, J.L., Darling, E.S., Ahmadia, G.N., Razak, T.B., 2019. Rebuilding coral reefs: success (and failure) 16 years after low-cost, low-tech restoration. Restor. Ecol. 27 (4), 862–869. Frederick, P., Vitale, N., Pine, B., Seavey, J., Sturmer, L., 2016. Reversing a rapid decline in oyster reefs: effects of durable substrate on oyster populations, elevations, and aquatic bird community composition. J. Shellfish Res. 35 (2), 359–367. Kendrick, G.A., Marbà, N., Duarte, C.M., 2005. Modelling formation of complex topo graphy by the seagrass Posidonia oceanica. Estuar. Coast. Shelf Sci. 65 (4), 717–725. Lee, K.S., Park, J.I., 2008. An effective transplanting technique using shells for restoration of Zostera marina habitats. Mar. Pollut. Bull. 56 (5), 1015–1021. Liversage, K., Chapman, M.G., 2018. Coastal ecological engineering and habitat re storation: incorporating biologically diverse boulder habitat. Mar. Ecol. Prog. Ser. 593, 173–185. Marbà, N., Duarte, C.M., 1995. Coupling of seagrass (Cymodocea nodosa) patch dynamics to subaqueous dune migration. J. Ecol. 83, 381–389. Marbà, N., Duarte, C.M., 1998. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 174, 269–280. Meinesz, A., Caye, G., Loques, F., Molenaar, H., 1993. Polymorphism and development of Posidonia oceanica transplanted from different parts of the Mediterranean into the National Park of port-Cros. Bot. Mar. 36, 209–216. Menna, M., Poulain, P.M., Ciani, D., Doglioli, A., Notarstefano, G., Gerin, R., Rio, M.H., Santoleri, R., Gauci, A., Drago, A., 2019. New insights of the Sicily Channel and southern Tyrrhenian Sea variability. Water 11, 1355. Molenaar, H., Meinesz, A., 1995. Vegetative reproduction in Posidonia oceanica: survival and development of transplanted cuttings according to different spacings, arrange ments and substratum. Bot. Mar. 38, 313–322. Morris, R.L., Konlechner, T.M., Ghisalberti, M., Swearer, S.E., 2018. From grey to green: efficacy of eco-engineering solutions for nature-based coastal defence. Glob. Change Biol. 24 (5), 1827–1842.
6. Conclusions Two ecological processes, namely re-colonization and habitat frag mentation, can sometimes lead to a similar landscape. When only a snapshot of a process is available, the possibility of mistaking the actual ongoing process is very high. This is what possibly took place when Calvo et al. were shown pictures of the P. oceanica circular patches at Capo Feto by the team of Biosurvey S.r.l., an academic spin-off of the University of Palermo which performed the transplantation operations. The presence of a very large number of seedlings on the sea bottom due to the abnormally great production and release of seeds by the western Sicilian P. oceanica meadow between spring and summer 2019 very likely contributed to the erroneous conclusion that the patches ob served were the result of seedling colonization. Regarding the restoration of damaged P. oceanica beds we agree that further impacts to, and consequent loss of the existing meadows should be avoided as much as possible, if not prevented completely. We believe that knowledge of the ecology of seagrasses and of P. oceanica needs to be improved. The natural recovery of P. oceanica on rubble mounds observed for several years at Capo Feto prompted research on the co lonization process and on the possibility of restoring heavily impacted areas to conditions similar to those the species found once the coloni zation started. We still have a long way to go before we can predict the outcome of a restoration action. The Capo Feto experience has provided the chance to identify some habitat features which are conducive to successful P. oceanica meadow recovery. The presence of these features should be recommended at sites targeted for restoration actions in order to im prove the likelihood of positive transplantation outcomes. References Alagna, A., Vega Fernández, T., Terlizzi, A., Badalamenti, F., 2013. Influence of micro habitat on seedling survival and growth of the Mediterranean seagrass Posidonia oceanica (L.) Delile. Estuar. Coast. Shelf Sci. 119, 119–125. Alagna, A., Vega Fernández, T., Anna, G.D., Magliola, C., Mazzola, S., Badalamenti, F., 2015. Assessing Posidonia oceanica seedling substrate preference: an experimental determination of seedling anchorage success in rocky vs. sandy substrates. PLoS One 10 (4), e0125321. Alagna, A., D'Anna, G., Musco, L., Vega Fernández, T., Gresta, M., Pierozzi, N., Badalamenti, F., 2019. Taking advantage of seagrass recovery potential to develop novel and effective meadow rehabilitation methods. Mar. Pollut. Bull. 149, 110578. Alagna, A., Zenone, A., Badalamenti, F., 2020. The perfect microsite: how to maximize Posidonia oceanica seedling settlement success for restoration purposes using ecolo gical knowledge. Mar. Environ. Res. 161, 104846. Badalamenti, F., Di Carlo, G., D’Anna, G., Gristina, M., Toccaceli, M., 2006. Effects of dredging activities on population dynamics of Posidonia oceanica (L.) Delile in the Mediterranean Sea: the case study of capo Feto (SW Sicily, Italy). Hydrobiologia 555, 253–261. Badalamenti, F., Alagna, A., D’Anna, G., Di Stefano, G., Vega Fernández, T., 2010. Sperimentazone di metodologie di facilitazione del reclutamento di germogli di Posidonia oceanica finalizzate al ripristino delle praterie. Rapporto Tecnico, contratto n. 524645 del 26/07/2010. Consulenza scientifica nel campo del ripristino delle praterie di Posidonia oceanica per SAIPEM S.p.A. IAMC-CNR. U.O.S. di Mazara del Vallo, Sede distaccata di Castellammare del Golfo, Trapani, Italy, pp. 1–81. Badalamenti, F., Alagna, A., D’Anna, G., Terlizzi, A., Di Carlo, G., 2011. The impact of dredge-fill on Posidonia oceanica seagrass meadows: regression and patterns of re covery. Mar. Pollut. Bull. 62, 483–489. Badalamenti, F., Alagna, A., Fici, S., 2015. Evidences of adaptive traits to rocky substrates undermine paradigm of habitat preference of the Mediterranean seagrass Posidonia oceanica. Sci. Rep. 5 (1), 1–6. Balestri, E., Piazzi, L., Cinelli, F., 1998. Survival and growth of transplanted and natural seedlings of Posidonia oceanica (L.) Delile in a damaged coastal area. J. Exp. Mar. Biol. Ecol. 228 (2), 209–225. Balestri, E., Vallerini, F., Lardicci, C., 2017. Recruitment and patch establishment by seed in the seagrass Posidonia oceanica: importance and conservation implications. Front. Plant Sci. 8, 1067.
7
Marine Pollution Bulletin 161 (2020) 111754
Correspondence Ng, C.S.L., Toh, T.C., Chou, L.M., 2017. Artificial reefs as a reef restoration strategy in sediment-affected environments: insights from long-term monitoring. Aquat. Conserv. 27 (5), 976–985. O’Connor, M.I., Violin, C.R., Anton, A., Ladwig, L.M., Piehler, M.F., 2011. Salt marsh stabilization affects algal primary producers at the marsh edge. Wetl. Ecol. Manag. 19 (2), 131–140. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L., Hughes, R.A., Kendrick, G.A., Kenworthy, W.J., Olyarnik, S., Short, F.T., Waycott, M., Williams, S.L., 2006. A global crisis for seagrass ecosystems. BioScience 56, 987–996. Park, J.I., Lee, K.S., 2010. Development of transplantation method for the restoration of surfgrass, Phyllospadix japonicus, in an exposed rocky shore using an artificial un derwater structure. Ecol. Eng. 36 (4), 450–456. Pereda-Briones, L., Infantes, E., Orfila, A., Tomas, F., Terrados, J., 2018. Dispersal of seagrass propagules: interaction between hydrodynamics and substratum type. Mar. Ecol. Prog. Ser. 593, 47–59. Pereda-Briones, L., Terrados, J., Agulles, M., Tomas, F., 2020. Influence of biotic and abiotic factors of seagrass Posidonia oceanica recruitment: identifying suitable mi crosites. Mar. Environ. Res. 105076. Piazzi, L., Balestri, E., Magri, M., Cinelli, F., 1998. Experimental transplanting of Posidonia oceanica (L.) Delile into a disturbed habitat in the Mediterranean Sea. Bot. Mar. 41 (1–6), 593–602. Piazzi, L., Acunto, S., Cinelli, F., 1999. In situ survival and development of Posidonia oceanica (L.) Delile seedlings. Aquat. Bot. 63 (2), 103–112. Pirrotta, M., Tomasello, A., Scannavino, A., Di Maida, G., Luzzu, F., Bellissimo, G., Bellavia, C., Costantini, C., Orestano, C., Sclafani, G., Calvo, S., 2015. Transplantation assessment of degraded Posidonia oceanica habitats: site selection and long-term monitoring. Mediterr. Mar. Sci. 16 (3), 591–603. Sintes, T., Marbà, N., Duarte, C.M., 2006. Modeling nonlinear seagrass clonal growth: assessing the efficiency of space occupation across the seagrass flora. Estuar. Coasts 29 (1), 72–80. Telesca, L., Belluscio, A., Criscoli, A., Ardizzone, G., Apostolaki, E.T., Fraschetti, S., Gristina, M., Knittweis, L., Martin, C.S., Pergent, G., Alagna, A., Badalamenti, F., Garofalo, G., Gerakaris, V., Pace, M.L., Pergent-Martini, C., Salomidi, M., 2015. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep. 5, 12505. Temmerman, S., Meire, P., Bouma, T.J., Herman, P.M., Ysebaert, T., De Vriend, H.J., 2013. Ecosystem-based coastal defence in the face of global change. Nature 504 (7478), 79–83. Terrados, J., Marin, A., Celdrán, D., 2013. Use of Posidonia oceanica seedlings from beach-
cast fruits for seagrass planting. Bot. Mar. 56 (2), 185–195. Tomasello, A., Pirrotta, M., Calvo, S., 2019. Construction underwater landscape by using Posidonia oceanica transplanting combined with innovative artificial reefs. In: Proceedings of the 6th Mediterranean Symposium on Marine Vegetation, Antalya,Turkey, 14–18 January 2019, pp. 92–96. http://www.rac-spa.org/sites/ default/files/symposium/proceedings_msmv_2019_final.pdf. van Katwijk, M.M., Hermus, D.C.R., 2000. Effects of water dynamics on Zostera marina: transplantation experiments in the intertidal Dutch Wadden Sea. Mar. Ecol. Prog. Ser. 208, 107–118. Vangeluwe, D., 2007. Effets de la transplantation sur la biométrie et sur la dynamique des nutriments, du carbone et de la chlorophylle de Posidonia oceanica (L.) Delile. M.Sc. Thesis. University of Liège. Vega Fernández, T., Milazzo, M., Badalamenti, F., D’Anna, G., 2005. Comparison of the fish assemblage associated with Posidonia oceanica after the partial loss and con sequent fragmentation of the meadow. Estuar. Coast. Shelf Sci. 65 (4), 645–653. Verdura, J., Sales, M., Ballesteros, E., Cefalì, M.E., Cebrian, E., 2018. Restoration of a canopy-forming alga based on recruitment enhancement: methods and long-term success assessment. Front. Plant Sci. 9, 1832. Walles, B., Troost, K., van den Ende, D., Nieuwhof, S., Smaal, A.C., Ysebaert, T., 2016. From artificial structures to self-sustaining oyster reefs. J. Sea Res. 108, 1–9.
Adriana Alagnaa,b, , Giovanni D'Annaa, Luigi Muscob, Tomás Vega Fernándezb, Martina Grestac, Natalia Pierozzic, Fabio Badalamentia,b,d a CNR-IAS, Institute for the study of Anthropic Impacts and Sustainability of the Marine Environment, Via G. da Verrazzano 17, 91014 Castellammare del Golfo, TP, Italy b Stazione Zoologica Anton Dohrn, Integrative Marine Ecology Department, Villa Comunale, 80121 Naples, Italy c Saipem S.p.A., via Martiri di Cefalonia 67, 20097 San Donato Milanese, MI, Italy d School of Geosciences, Grant Institute, King's Buildings, University of Edinburgh, Edinburgh, United Kingdom E-mail address: [email protected] (A. Alagna). ⁎
⁎ Corresponding author at: CNR-IAS, Institute for the Study of Anthropic Impacts and Sustainability of the Marine Environment, Via G. da Verrazzano 17, 91014 Castellammare del Golfo, TP, Italy.
8