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Degree of Master of Science in Marine Biological Resources (IMBRSea)

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University of Ghent
Host organization: Università Politecnica delle Marche
Assessing the effectiveness of different
transplantation methods for the red coral
Corallium rubrum in the Ligurian Sea
Master Thesis
Juliette Villechanoux
Promotor: Carlo Cerrano
Supervisor : Torcuato Pulido Mantas
Degree of Master of Science in Marine Biological Resources (IMBRSea)
Academic year: 2021-2022
Report due date: 05/01/2022
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Summary
Executive Summary ................................................................................................................................. 4
Abstract ................................................................................................................................................... 5
1. Introduction & Aims ............................................................................................................................ 6
1.1 Ecology of shallow Corallium rubrum populations ................................................................. 6
1.2 History of Corallium rubrum ................................................................................................... 7
1.3 Harvest of Corallium rubrum since the 1800s and its consequences on shallow populations’
structure .............................................................................................................................................. 9
1.4 Differences between deep and shallow Corallium rubrum populations .............................. 10
1.5 Protection status of Corallium rubrum ................................................................................. 11
1.6 Restoration of Corallium rubrum .......................................................................................... 12
1.7 MERCES project ..................................................................................................................... 12
1.8 Aims of the study .................................................................................................................. 13
2. Material and Methods ...................................................................................................................... 14
2.1 Literature research ................................................................................................................ 14
2.2 Study sites ............................................................................................................................. 14
2.3 Transplantation methods ...................................................................................................... 15
2.3.1 Colonies collection ............................................................................................................... 15
2.3.2 Transplantations in crevices ................................................................................................. 16
2.3.3 Transplantations on rocks .................................................................................................... 16
2.3.4 Transfer of colonies and settlers from shallow to deep waters .......................................... 16
2.4 Data collection ............................................................................................................................ 17
2.4.1 Underwater surveys ............................................................................................................. 17
2.4.2 Apical fragments .................................................................................................................. 18
2.5 Data analysis ............................................................................................................................... 18
2.5.1 Data sorting .......................................................................................................................... 18
2.5.2 2D analysis ........................................................................................................................... 18
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2.5.3 Skeleton structural study ..................................................................................................... 19
2.5.4 Statistical analysis ................................................................................................................ 19
3. Results ............................................................................................................................................... 21
3.1 Review on past C. rubrum transplantations and larval enhancement experiments ............ 21
3.2 Transplantation techniques in shallow waters ..................................................................... 21
3.2.1 Survival, detachment and death of transplants ................................................................... 21
3.2.3 Height growth of transplants ............................................................................................... 25
3.3 Transfer of colonies and settlers from shallow to deep waters ................................................ 26
3.3.1 Survival and detachment of transplants .............................................................................. 26
3.3.2 Survival of shallow settlers and settlement of deep settlers ............................................... 26
3.4 Scleraxis structure of apical parts ............................................................................................... 28
4. Discussion .......................................................................................................................................... 30
5. Conclusion ......................................................................................................................................... 32
Acknowledgements ............................................................................................................................... 33
Appendix ............................................................................................................................................... 34
References ............................................................................................................................................ 38
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Executive Summary
The long-living Mediterranean gorgonian Corallium rubrum is a key engineering species in the
coralligenous bioconstructions and a highly exploited species. Due to its small growth rate the
historical harvest of its red calcium carbonate skeleton led to depletion of shallow banks and modified
its population structure drastically. Deeper populations that are still poorly known ecologically are
now in danger even though measures have been taken to limit harvest impact. In order to manage
this resource effectively more efforts have to be implemented to restore and protect C. rubrum
population, especially in areas where natural recovery is unlikely. One way is to use transplantation
techniques which have been increasing in the past decade to restore Mediterranean octocorals. But
C. rubrum particularity is to grow under crevices and caves above 60 m depth, and the few
experiments carried out so far to transplant it have only be done in an erected position mostly using
a two-component epoxy putter. Therefore this study investigates suitable techniques for the
successful transplantation of this species by reviewing previous transplantation experiments and by
presenting six different transplantation techniques conducted in the Ligurian Sea. Transplantation
under crevices is conducted for the first time using two different techniques to maintain the
fragments: a PVC grid or polystyrene packaging, both in combination with an epoxy putty. Two other
transplantations were done in an erected position using either a PVC grid with the epoxy putty or just
the epoxy putty. Results show that the PVC grid method is a promising technique (survival rate of 60%
in an erected position and of 32% under crevices) requiring further improvement and assessment to
reach a higher percentage of survivors and guarantee an effective restoration. A transfer of shallow
colonies and settlers from 30 to 70 m depth was also tested as a transplantation technique to restore
deeper populations. The high survival rate observed of transplanted colonies (82%) reveals that
shallow colonies can survive in deeper environments as well as shallow recruits (average survival rate
of 33%). Furthermore, adaptative capabilities of shallow C. rubrum colonies to cope with
environmental changes are highlighted with the observation of a fragmentation like-process in C.
rubrum branches. It was observed in situ in and deduced by SEM observations in transplanted
colonies.
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Abstract
Corallium rubrum has been exploited by humankind for centuries. The long-term exploitation
dynamics of this species make it ever more important today to increase protection and restoration
efforts, especially in areas where natural recovery is hindered or unlikely. So far, only very few
experiments were carried out in the past investigating suitable techniques for the successful
transplantation of this species. For this reason, a review was conducted in order to synthesize previous
results and identify most promising methodologies. Additionally, unpublished data of six different
transplantation techniques was analysed and discussed in the context of the review. Five techniques
used fragments for transplantation while one used newly settled larvae on PVC-tiles. C. rubrum often
grows upside down under crevices and rims as well as in caves making the transplantation of
fragments comparatively challenging. For the first time, C. rubrum was transplanted upside down and
using a PVC-grid in combination with an epoxy putty to hold fragments in place showed promising
results. Further, adaptive capabilities of this species were discovered as a potential response to
changing environmental conditions.
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1. Introduction & Aims
Coralligenous reefs are temperate bioconstructions formed by coralline algae at low light levels and
by sessile animal taxa (Ballesteros 2006; Ingrosso et al. 2018). In the Mediterranean coralligenous
assemblages, gorgonian corals are among the main components and provide three-dimensional
complexity by forming patches of dense canopies called animal forests, enhancing local biodiversity
(Gili & Coma 1998; Ballesteros 2006; Rossi 2013; Guizien & Ghisalberti 2016). They are slow-growing,
long-lived keystone species considered one of the most efficient suspension feeders in extracting and
processing energy from water column thanks to their capture of seston via their three-dimensional
fans. For this reason, they play a vital role in transferring energy from the less stable planktonic system
to the more stable benthic one (Gili & Coma 1998; Sebens et al. 2016; Rossi 2017).
1.1 Ecology of shallow Corallium rubrum populations
One of these coralligenous bioconstructions key engineering gorgonian species is the red coral
Corallium rubrum (Linnaeus, 1758) (Teixidó et al. 2011; Kipson et al. 2011). Part of the Corallidae family
or precious corals, its skeleton is composed of solid carbonate giving it its hard structure, which is
unusual for gorgonians. It is endemic to the Mediterranean Sea and found along Atlantic areas, living
on vertical cliffs, crevices and caves from 20 to 200 m depths and can be found down to 1,000 m depth
(Zibrowius et al., 1984; Costantini et al. 2016). Although it has a species with a wide bathymetric
distribution, the current knowledge is based on shallow populations (20 to 50 m depth).
Figure 1. The Mediterranean gorgonians species Corallium rubrum in an upside down position (Credits: Carlo Cerrano)
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It is a slow-growing, gonochoric (Lacaze-Duthiers 1864) species with a time-limited asexual
reproduction in summer, low polyp fecundity with less than one larvae produced per polyp
(Santangelo et al. 2003; Tsounis et al. 2006; Torrents & Garrabou 2011) and high recruitment densities
(Bramanti et al. 2005; 2014; Benedetti et al. 2011; Santangelo et al. 2012; Costantini et al. 2018).
Colonies can already be fertile at 2 cm tall, with the smallest one discovered being 1.5 cm and optimum
fertility reached at 6 cm height (Torrents et al. 2005; Tsounis et al. 2006).
Its colony growth rate and life span are still not fully resolved but findings reach up to 200 years old
(Teixidó et al. 2011), placing it among the longest-living organisms in the Mediterranean benthic
assemblages (Ballesteros 2006). During early coral stages, growth rate is found to be more variable
and possibly higher than adult stages (Costantini et al. 2018). Its growth rate can be averaged to 0.6
mm·y-1 in basal diameter and 1 cm·y-1 in height taking decades for a big valuable colony to form and
hundreds of years for a forest to form (Bavestrello et al. 2009; Cerrano et al. 2013, supplementary
table S2).
1.2 History of Corallium rubrum
Not only C. rubrum is important for Mediterranean benthic assemblages, but it also has a high socio-
cultural and economic valuation hence the scientific community’s interest in this species. The precious
red coral has been fished for millennia for its red calcium carbonate skeleton used for precious
artifacts production (Tescione 1973; Cicogna & Cattaneo-Vietti 1993), making it one of the most
valuable harvested living marine resources (Bruckner 2014). It exceeded decoration purposes as it was
also believed to be a symbol of protection for good health and good luck (Ascione, 2010).
Figure 2. The antique ingegno (left) composed of two wooden bars forming a cross and equipped with nets to entangle
red coral colonies while it was dragged by boats. The modern “ingegno” (right) used by motorboats and composed of a
metallic bar equipped with multiple nets.
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The discovery of polished perforated red coral beads in Germany dating from 25,000 years ago
(Tescione 1965) and vestiges of 26,000 years old found in the oldest French port Marseilles (Harmelin
2010), testify how old the harvest and trade of this species is. Its use exceeded the Mediterranean
basin through the “silk route” and “spice route” reaching India, Central Asia, China and the Arabian
peninsula (De Simone 2010). In ancient Greece, sponge divers selectively harvested C. rubrum before
using iron hooks or “kouralio” in deeper waters. The technique improved around 1000 AD with
“ingegno” or St. Andrews Cross device invented by Arabs to entangle coral in nets and was further
refined in Italy in the late 1800s (Figure 2) (Bruckner 2009). This red coral monopoly was held by
Mediterranean civilizations (Figure 3), favoring their development throughout the centuries.
Nowadays the global center of Corallium artifact production is Torre del Greco in Italy, with annual
revenues of US $200 million (Bruckner 2009).
The trade and harvest which started millennia ago have to be taken into account when studying
current C. rubrum populations. Ancestral humans’ fishing activity completely changed how this species
was originally distributed and structured before. Current researches on red coral are based on the
impacted species nowadays populating the Mediterranean sea. From the data we can compare it to,
meaning from already impacted populations, Corallium rubrum is not currently disappearing but
populations are certainly decreasing (see next chapter).
Figure 3. Principal red coral commercialization centres throughout the centuries. The monopoly was held by
Mediterranean civilizations, favouriting their development throughout the centuries.
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1.3 Harvest of Corallium rubrum since the 1800s and its consequences on
shallow populations’ structure
Even though its harvest and trade began more than 20,000 years ago, it reached its first peak in the
1800s (Bruckner 2014). Historically effort and landings followed boom and bust” cycles: every time a
new precious bank was discovered, it was quickly depleted resulting in drastic increase in landings
followed by sharp declines (Tescione 1973; Fujioka 2008). By the 1970s fishing methods improved and
bigger vessels were used, resulting in greater damages of coralligenous habitats with the use of metal
dredges reaching deeper (180 m) intact areas (Chessa & Cudoni 1988; FAO 1988; Bruckner 2014).
Simultaneously, selective harvest through SCUBA diving developed allowing fishermen to reach for
colonies hidden in crevices and caves previously inaccessible (Liverino 1989). This resulted in a
dramatic size shift in shallow waters population from banks previously dominated by large branched
colonies of 30-50 cm height (10-30 mm diameter) to populations dominated by small colonies of 3-5
cm height (5-7 mm diameter) as we can see in figure 4 (Liverino 1983; Garrabou & Harmelin 2002;
Tsounis et al. 2006a). Shallow populations were transformed from “forest-like” structures to “grass
plain-like” instead (Tsounis et al. 2006b).
Figure 4. (a,b) A red coral population discovered between 18 and 27 m in the Scandola Marine Reserve in 2010 with a high
density (201 colonies·m2) of large colonies (9.4 cm in height). (c) Typical red coral population from a MPA (Scandola) a low
density (70 colonies·m2) of large colonies (6.7 cm in height) (d) Standard population from an unprotected area with a high
density (466 colonies·m2) of small colonies (2.3 cm in height).
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Despite the fishing techniques improvement, red coral landings showed sharp declines in the 1980s
(Figure 5) alarming the UN Food and Agriculture Organization’s General Fisheries Commission for the
Mediterranean (FAO GFCM) that resulted in multiple decisions through the years: a quota
establishment (1983), a 7 mm minimum diameter for harvest (1983) at the trunk with a maximum
tolerance limit of 10% in live weight of undersized colonies (2012) and a ban on dredges use
(Mediterranean wide in 1994) making SCUBA diving the only legal harvesting method (FAO 1983,
1988; Council of the European Union 1994; GFCM 2011; Bruckner 2014). With the depletion of shallow
populations and the minimum harvest size, divers harvest now deeper unexploited banks up to 130
depths to find large valuable colonies thanks to mixed-gas SCUBA diving (Costantini 2019). Additionally
to SCUBA diving, there is a current pressure made by the harvesters to use Remotely Operated
Vehicles (ROV) to harvest below 130 m depth (Constantini et al. 2016). But these populations (50-200
m depth) are still poorly known ecologically with little research on them (Torrents et al. 2008; Priori
et al. 2013 and references herein; Cau et al. 2016) and based on historical events their large branched
colonies will not last very long if no better management is done to protect them.
1.4 Differences between deep and shallow Corallium rubrum populations
Due to its large range of distribution, shallow and deep populations of C. rubrum are exposed to
different anthropogenic pressures but also to different ecological variables which may affect
population structure and dynamics (Garrabou et al. 2002), as well as genetic diversity.
For starters, the deepest banks experience stable temperatures whereas shallow ones are exposed to
higher, more variable temperatures and have to endure climate change consequences. Indeed, C.
Figure 5. Global catch data for the Mediterranean red coral between 1963 and 2011. Data are shown for the six primary
source countries; six other reporting countries are listed as ‘other’ (Bruckner 2014)
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rubrum banks above 30 m depth were affected by mass mortality episodes caused by positive
seawater temperature anomalies in 1999 and 2003 in the North-western Mediterranean sea, with
sometimes, more than 80% of colonies affected (Cerrano et al. 2000b, 2008; Garrabou et al. 2009).
Additionally, 5 m depth colonies experience seawater temperature fluctuation rates of 10°C in 24h,
with 25°C as a maximum value (Haguenauer et al. 2013). This shallow harvested heterogeneous
habitat affecting size and shape of the colonies with the observation of autotomy of the branch tips
during thermal anomalies (Russo et al., 1999) largely differs from the deep stable one. Therefore,
shallower colonies are more resistant and adapted to marginal environmental conditions than
mesophotic ones (Ledoux et al. 2015).
Furthermore, Costantini et al (2011, 2016) revealed the presence of a genetic diversity threshold at
40-50 m depth differing shallow populations from deeper ones, suggesting that depth may have a role
in determining genetic differentiation in these populations. The first shows higher genetic variability
and a strong genetic structure pattern, driven by the limited dispersal ability of the red coral planulae
(Weinberg 1979a). This threshold could be explained by different barriers: shifts in the spawning
period creating a gene flow barrier (deeper water colonies’ spawning occurs later) and the presence
of a thermocline acting as a physical barrier for settlers and recruits dispersal. Genetic structure could
be related to how shallow colonies respond to thermal stress affecting their adaptive abilities to
respond to environmental changes due to climate change. These plus other findings of genetic data
on C. rubrum populations suggest limited connectivity in this species (Ledoux et al. 2010) even though
the larvae has a dispersal potential over several km (Martinez-Quintana et al. 2015), most probably
determining in the highly fragmented seascape of deepwater populations (Cau et al. 2016).
On top of these differences, Corallium rubrum population structure follows a depth-related
distribution with higher sparsely distributed colonies in deeper environments (80-170 m depth) and
shows an inverse relationship between maximum population density and mean colony height
according to a study performed in southern Sardinian waters. Therefore, the red coral population
structure may be shaped by a self-thinning process through recruitment limitation, where immature
or disturbed populations display a “grass-plain like” structure whereas mature or stable populations
display a “forest-like” structure. It coincides with current shallow population structure highly
disturbed due to high anthropogenic pressure.
1.5 Protection status of Corallium rubrum
Despite the historical intensive harvesting pressure on this species, C. rubrum is not considered a
threatened species but an endangered one by IUCN. But the Corallium genus is not included in
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Appendix II of the Convention on the Trade in Endangered Species (CITES) despite two proposals in
the past years from the US and EU to list all its species (CITES 2007, 2010). On the other hand, it is
included in international conventions suggesting controlled harvesting of corals (SPAMI, Annex III;
Berna, Annex, III; Habitat Directive, Annex V; Barcelona Convention) and GCFM (2014) promoted the
definition of a Regional Management Plan for the Mediterranean Sea.
1.6 Restoration of Corallium rubrum
With a highly altered population structure in the Mediterranean sea, scientists agree that efforts are
needed to restore and resource previously inhabited areas for a better management of this resource,
and restore the ecosystem services this species provided, which are often still poorly documented.
Researches on Mediterranean octocorals restoration techniques are increasing in the past decade
based on transplantation methods (Linares et al. 2008; Fava et al. 2009; Montero-Serra 2018; Casoli
et al. 2021), and previous transplantation experiment of C. rubrum confirmed the potential success of
this restoration action and strongly support the feasibility of these techniques at local spatial scales
(Montero-Serra et al. 2018). Transplanted populations should be viable in the long term with
reproduction reaching annual rates due to the limited larval dispersal and high self-recruitment rates
of the species. But to manage and restore this species effectively, one has to take into account that it
consists of an array of metapopulations, structured both geographically and by depth (Constantini et
al. 2016). Therefore creation of Marine Protected Areas reaching deep red coral banks is
recommended as a precautionary conservation tool and has proven to help restore previously
harvested banks (Bavestrello et al. 2015).
1.7 MERCES project
Among restoration work and studies on red coral, one can find the Marine Ecosystem Restoration in
Changing European Seas (MERCES) Project (2016 to 2020) focusing on the restoration of the most
vulnerable and fragile marine habitats (seagrass meadows, algal and kelp forests, coralligenous
outcrops, cold-water corals, canyons, seamounts and fjords) on a multi-regional approach from Turkey
to Norway. It allowed to test and set up different restoration protocols for each targeted habitat with
its corresponding selected species. In combination with other gorgonians, Corallium rubrum was used
to restore hard bottoms in the coralligenous outcrops habitat in the Catalan coast (Spain), Ligurian
Sea (Italy) and Croatia (MERCES 2007, 2021). The C. rubrum transplantations studied in this thesis
were initially conducted as part of the MERCES project.
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1.8 Aims of the study
A comprehensive and synthetized work of transplantation methods and larvae recruitment
experiments on Corallium rubrum is currently lacking in today’s literature. Therefore, the goal of this
study is to provide an overview and guidance on transplantation techniques of Corallium rubrum to
help future restoration projects. It is achieved by first compiling information on transplantation
techniques and larvae enhancement experiments of red coral and secondly by performing a case study
of six transplantation techniques of Corallium rubrum, including one of larvae settlement in the
Ligurian Sea. The objective is to analyse the effectiveness of each method and if transferred shallow
colonies and juveniles can survive in deeper waters by analysing (i) survival rate and colony loss rate,
(ii) appearance of new branches, (iii) pattern of growth variations, (iv) fragments under a microscope
and by comparing the results with previous methods.
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2. Material and Methods
2.1 Literature research
A precise literature research was conducted on transplantation experiments of Corallium rubrum in
order to identify the state-of-the-art knowledge on its transplantation techniques. It was conducted
in the first weeks of thesis work. Online libraries (Web of Science, Google Scholar and Scopus) were
first used using specific keywords terminology (see Table 1) related to transplantation and to
techniques used in this thesis project. Scientific papers were selected according to the criteria of
having transplantation, recruitment or settlement experiments mentioned in their abstract. Due to
poor results on finding online literature older than 2000, research was extended with books and grey
literature. It allowed extending the study to Italian and French publications from the 1990’s non-
available online. All useful information found in the selected literature was synthetized in order to
create a database to refer and compare to when studying and mentioning C. rubrum transplantation
techniques.
Table 1. Sources and platform used for literature research
2.2 Study sites
Two localities were chosen in the Ligurian sea to perform six different transplantation experiments:
Gallinara Island, which submerged cavities and overhangs favour the development of red coral at
shallow depths, and Portofino Marine Protected Area. This choice was made according to two criteria
Source type
Source name
Online library
Google Scholar
Online library
Scopus
Online library
Web of Science
Report
Il Corallo, L'Oro Rosso del Mediterraneo (Bollettino Dei
Musei E Degli Istituti Biologici dell'Universita di Genova,
Volume 64-65, 1998-1999)
Report
Association Monégasque pour la Protection de la Nature:
Expériences de coralliculture en milieu naturel (1988)
Book
Red Coral and other Mediterranean Octocorals: Biology
and Protection (Ministerio per le Politiche Agricole,
Roma, 1999)
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following MERCES restoration protocol: (i) existence of historical data of red coral for an eligible
restoration site and (ii) knowledge of degradation causes of red coral and evaluation of actual
anthropogenic stressors.
Availability of scientific records are generally scarce and complicated to find with online research tools.
First scientific works on red coral in the Ligurian sea led by Issel (1884) and Parona (1898) report
populations in Gallinara Island and Portofino. Gallinara red coral banks are suspected to have
disappeared due to excessive fishing efforts (Marchetti 1965 a, b) but restoration efforts were put into
place as it was the location for the first transplantation experiments led by Cerrano in 1997 and 2000.
The red coral population of Portofino is well known and documented with a positive impact of the
MPA in red coral colonies (Bavestrello et al. 2015; Bramanti et al. 2014; Cattaneo-Vietti & Bavestrello,
2010; Marchetti 1965). With the creation of the Portofino MPA in 1999, underwater fishing activity
became illegal ending the intense harvesting pressure led by SCUBA divers from the 1950s to the late
1970s (Bavestrello et al. 2015). As for Gallinara Island, underwater and boat fishing activities are still
allowed but transplants were put under crevices minimizing the risk of being damaged by boat
activities.
2.3 Transplantation methods
Four transplantation experiments were carried out in Gallinara Island at 30 m deep: two in crevices
where fragments were hanging down and two on rocks where fragments were erected in order to see
the difference of transplanting in crevices or rocky substrate. Two other transplantations were carried
out in Portofino MPA transferring red coral on an open wall and larval recruits on PVC tiles from 30 m
to 70 m depth. Colonies were fixated on the coralligenous substrate using a non-toxic two-component
epoxy putty (Veneziani) as glue that takes one hour to dry.
2.3.1 Colonies collection
Apical fragments of Corallium rubrum were collected in shallow waters in Portofino by SCUBA diving
from mature, healthy, branched donor specimen colonies and put into sealed plastic bags. A colony
was considered healthy when less than 10% of its tissue was affected by necrosis and/or epibiosis
Collection was made in the shallowest banks in order to select the most tolerant donors. As male and
female gorgonians cluster together, donor specimens were chosen from scattered colonies to ensure
in transplanting male and female fragments to guarantee reproduction. Due to C. rubrum fragility,
fragments were broken by pinches to obtain the cleanest cut possible. Back to the surface, plastic bags
were placed in coolers (16-21°C environment) for transportation to the restoration location.
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Fragments for each transplantation method were always collected following the same protocol, with
the exception of the donor site for the larval enhancement method, which is described further below,
and for the transfer of colonies from 30 m to 70 m depth. For the latter, newly settled larvae were
collected at 30 m depth in a marine cave instead of shallow banks. More details on the methodology
and necessary material can be found in MERCES Deliverable D3.2.
2.3.2 Transplantations in crevices
Polystyrene method
In August 2017, 20 colonies were transplanted by SCUBA diving in Gallinara Island at 30 m depth into
small crevices and holes. Coralligenous substrate surface was first cleaned using a metal brush to
ensure better adherence. The two-component epoxy putty was prepared by mixing equal parts by
hands of the two components and put on the substrate. Corallium rubrum colonies were directly
placed into the glue as its rigid scleraxis increase adhesion. Colonies were attached in small patches
of 3 to 5 fragments. As the colonies were facing upside down or were in an unstable position,
polystyrene packaging was used to maintain them in place while the glue dried (Figure 6A). It was
removed a few hours later in another dive.
PVC grid method
In October 2017, another 25 colonies were transplanted by SCUBA diving in Gallinara Island at 30 m
depth into small crevices and holes following the same epoxy-putty protocol but modifying the
polystyrene step. To maintain colonies into place, a PVC grid was fixated to the substrate with metal
pegs on top of the epoxy putty (Figure 6B). Corallium rubrum colonies were inserted in the glue after
the grid installation. In total 3 grids were installed with 6 to 10 colonies in one grid.
2.3.3 Transplantations on rocks
In March 2018, 14 more colonies were transplanted by SCUBA diving in Gallinara Island at 30 m depth
on rocky substrate following the same epoxy putty protocol (Figure 6C). For 5 colonies a PVC grid was
put on top of the glue as done in the crevices’ transplantation (Figure 6D).
2.3.4 Transfer of colonies and settlers from shallow to deep waters
On open wall
In April 2018 39 big colonies were collected at 30 m depth in Portofino MPA near to the Colombara
Cave. They were transplanted on a vertical open coralligenous wall at 70 m depth in the same area
using the two-component epoxy putty (Figure 6E) and following the same epoxy-putty protocol as for
17
Gallinara transplantations. But since transplants were not facing upside down, no second component
was used to maintain them into place while the putty dried.
With white PVC tiles
In spring 2016, before the start of red coral spawning, six 20×20 cm white PVC tiles were fixed with
steel screws on the ceiling of Colombara cave in Portofino at 34 m depth as Costantini et al. (2018).
PVC was chosen due to previous success in larval enhancement experiments (Costantini 2018;
Kennedy et al. 2017). The tiles were left for two years in order to collect two cohorts of larvae (summer
2016 and summer 2017). In April 2018 they were transferred by SCUBA diving at 70 m depth in the
same location of the open wall and fixed vertically on it with steel screws to avoid sedimentation. To
limit larvae loss the tiles were transferred in a framed plastic box where they were maintained distant
from each other and stable (Figure 6F).
Figure 6. Images of the different transplantation techniques in shallow water directly after transplantation. (A) Polystyrene
method. (B) Grid under crevices method. (C) Epoxy putty on rocks method. (D) Grid on rocks method. (E) Shallow colonies
transplanted to deep water method. (F) Larval enhancement experiment on PVC tiles.
2.4 Data collection
2.4.1 Underwater surveys
Underwater visual census surveys and photographic samplings were carried out at each location after
transplantation to collect data on transplants and recruits settled on the PVC tiles. They were realized
by members of the Zoology laboratory of UNIVPM coordinated by Carlo Cerrano. A digital camera
(Canon G16) equipped with light was used to photograph each colony. In Gallinara island data was
A
B
C
D
E
F
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collected in August 2017, October 2017, November 2017, July 2018, September 2018, January 2019,
May 2019, August 2019, June 2021, September 2021 and November 2021. In Portofino, surveys were
done in April 2017, June 2018, September 2018 and October 2019. No surveys could be done in 2020
and early 2021 due to the COVID-19 pandemic.
2.4.2 Apical fragments
In November 2021, apical parts of transplants from Gallinara island were collected by SCUBA diving in
order to realize a skeleton structural study to analyse the sclerites and scleraxis. In total 14 fragments
from different transplants were carefully cut with metal pinches and put into sealed plastic bags. Back
at the surface, they were conserved in 90°C alcohol for transportation to the lab until experimental
procedure. In the same period, C. rubrum branches were collected at 25 and 35 m depth in Portofino
MPA (following the same procedure) to compare them with the transplanted ones. Each branch was
withdrawn from a different colony to minimize sampling impact and to provide the widest diversity of
C. rubrum populations. Some of these branches did not need to be cut with pinches as they were
beginning to detach themselves on their own from the colony similar to an autotomy procedure.
2.5 Data analysis
2.5.1 Data sorting
First step in analysing the data was to sort out all collected pictures from the underwater surveys since
the transplantations took place in Portofino and Gallinara. Each transplant was attributed a number
in order to identify it and a sequence of pictures of each transplant through time was built under
Microsoft PowerPoint to facilitate data visualization. The same procedure was done for the PVC tiles
but letters were attributed instead of numbers.
2.5.2 2D analysis
Photographic samples were used to analyse survival, detachment, death, height growth and changes
in the number of branches of transplants. The detachment or death of transplants was recorded
separately to identify if the loss was related to the transplantation methodology or to natural
mortality. A transplant was considered dead when it was completely affected by necrosis or by
epibiosis. If there were no photographic samples for 3 consecutive surveys the transplant was
considered lost. The branches were counted in each sample for each transplant. Software ImageJ
(Schneider et al. 2012) was used to measure transplants height but as no scale bar was included in the
19
pictures, PVC grid was used as a metric reference to scale (1 square = 1 cm). Height was measured
from the base to the highest point of the coral in a vertical plane.
Photographic samples of the PVC tiles were used to identify the initial number of shallow C. rubrum
settlers (i.e. larvae settled in the Colombara cave at 35 m depth from 2 cohorts present on the tile on
day 1 at 70 m depth), the number of deep C. rubrum settlers (i.e. larvae settled on the tiles during the
two years at 70 m depth after day 1), their survival and their density. It was not possible to estimate
the age of each settler since their height could not be measured. Density was defined as the number
of settlers per decimetre square.
2.5.3 Skeleton structural study
To assess C. rubrum skeleton health, the scleraxis (axial skeleton) and sclerites had to be dissociated
and all organic material removed. Thus collected apical fragments were soaked individually in tubes
in a 120 volume solution of peroxide oxygen (to reduce the risk to have artifact crystals) and heated
up carefully above a flame for 10 minutes twice to accelerate the dissociation and removal process.
The scleraxis were then individually separated from their sclerites in other tubes. All sclerites and
scleraxis were rinsed 3 times with reagent grade water (MilliQ) followed by a gradual alcohol
concentration rinsing (one time with 70%, 80%, 90%, 95% and 100%).
Scleraxis were first observed under a stereo-microscope with a focus on the apical and bottom parts
where they were cut or detached from the colony. Secondly, they were observed under a Scanning
Electron Microscope (SEM) to analyze the fine-scale scleraxis morphology and calcification formation.
Samples were mounted on aluminium stubs using carbon adhesive tabs and coated with gold (Au) for
five minutes using a Polaron Range sputter coater. Sclerites were put on coverslips with a pipette and
observed on the SEM following the same procedure as for the scleraxis. SEM observations were
conducted with a Philips® XL 20 microscope.
2.5.4 Statistical analysis
Survival rate (S) of transplants and settlers at a given survey was defined as
𝑆 = 𝑁𝑡
𝑁0
with Nt the number of living and attached transplants/settlers and N0 the total number of
transplants/settlers transplanted/present in the beginning.
20
Detachment rate (D) of transplants at a given survey was defined as
𝐷 = 𝐷𝑡
𝐷0
with Dt the number of detached transplants and D0 the total number of transplants transplanted in
the beginning.
Branching difference (B) of one transplant was defined as
𝐵 = 𝐵𝑙 𝐵0
𝐵0
with Bl the number of branches present in the last survey where the transplant was alive and B0 the
initial number of branches. Transplants detached in the second day of the experiments were not taken
into account.
Height growth (G) of transplants at a given survey was defined as
𝐺 = 𝐺𝑡 𝐺0
𝐺0
with Gt the measured height and G0 the initial transplant measured height in the first survey.
Transplants detached in the second day of the experiment were not taken into account.
Due to the low number of samples for the grid on rocks method, no statistical test was performed to
test the presence of a significant difference between the two different grid transplantation methods
for height growth. To test if there was a significant difference between the different transplantation
methods in Gallinara, a Kruskal-Wallis test was performed (data did not follow a normal distribution).
A Spearman’s correlation test was performed between the branching difference and the height
growth of transplants.
All statistical tests and most of the graphical content were performed on RStudio (R Development Core
Team 2008), the rest on Microsoft Excel
21
3. Results
3.1 Review on past C. rubrum transplantations and larval enhancement
experiments
A total of 10 scientific publications were found for C. rubrum transplantation experiments and 6 for
larval enhancement experiments (Appendix table A) all conducted in France, Italy or Spain and in
shallow waters (25-40 m depth). The first trial was carried out in situ in 1979 (Weinberg 1979b) with
very poor results (0% of survival) due to method failure causing transplants death (screws holding
fragments). In the next decade, three other attempts followed (Bianconi et al. 1988; Giacomelli et al.
1988; Arosio et al. 1989) but survival data is missing. In 1992 the first large-scale experiment
(Cattaneo-Vietti et al. 1992) on artificial substrate obtained survival rates of 40% with loss only due to
detachment. It was the first experiment using resin to fix transplants on the porphyry substrate. After
this study, resin became the main technique to attach C. rubrum transplants. Cerrano et al. (1997,
2000a) performed a series of transplantation experiments testing different substrates obtaining good
survival results for coralligenous environments. Since then, red coral transplantations are scarce with
only two further studies conducted (Ledoux et al. 2015; Montero-Serra et al. 2018). After a few
months survival rates were usually high with 100% (n=4 studies) of survival, but after 2 or 3 years on
an adequate substrate, it dropped to 71.5% (n=6 studies) on average. No previous experiment
transplanted red coral in an upside-down position under crevices, it was always transplanted in an
erected position.
The first larval enhancement experiment on tiles was carried out in 2000 (Cerrano et al. 2000b) and
since then it is a recurrent method to study settlement and recruitment density for C. rubrum
(Appendix Table B). Different materials were used such as limestone, cement, marble (n=3), PVC (n=2)
and even one with electrical currents. The average settlement density found across all publications
was 4.71±5.17 settlers·dm-2 with a minimum of 0 settlers·dm-2 and a maximum of 19.12 settlers·dm-2.
Only one study (Garrabou et al. 2002) examined this method over a longer time period (21 years)
which resulted in a considerably lower density of 0.9±0.3 colonies·dm-2.
3.2 Transplantation techniques in shallow waters
3.2.1 Survival, detachment and death of transplants
The survival rate after four years of C. rubrum transplanted under crevices was 30% (n=6) using the
polystyrene method and 32% (n=8) using the grid method.
22
For the colonies transplanted in an erected position on rocks, 33% (n=3) survived using the epoxy
putty method and 60% (n=3) using the grid method after three years and a half for both (Figure 7).
For the polystyrene method under crevices, a major decline was observed at the beginning of the
experiment with 15% (n=3) loss after one day and 40% (n=8) after two months due to detachment
(Figure 7). After these initial losses, the survival rate remained stable for one year. Another decline of
25% (n=6) was recorded after the year 2020 where no surveys could be conducted.
For the grid method under crevices, the first loss of transplants was observed only after one year with
a sharp decline of 52% (n=13) due to the fall of one of the grids resulting in the detachment of most
of its transplants (Figure 7). The decline persisted the following years with a loss of 12% (n=3) in 2020.
As for the grid method in erected position, the first loss was observed after five months (20%, n=1)
while after three years one of the grids detached leading to an additional loss of 20% from the initial
number of transplants.
Finally, the epoxy putty method on rocks showed the first loss of transplants after one year (11%, n=1)
and decline persisted the following years.
Loss of transplants was in majority due to method failure with the detachment of transplants from the
epoxy putty or because of grids falling. Indeed, detachment affected 70% of transplants using the
polystyrene method and 60% using the grid under crevices method, 40% using the grid on rocks
methods and 44% using the epoxy putty method (Figure 8). On the other hand, death affected only
5% (n=3) of all transplants: 4% (n=1) of transplants using the grid under crevices method and 22%
(n=2) of transplants using the epoxy putty method. The cause of death was due to full necrosis for the
latest (covered by coralline algae after three years) and to full epibiosis cover for the first (its size was
extremely small) (Figure 10). Two other transplants from the same epoxy putty method patch were
affected by partial necrosis and survived. In total, epibiosis affected 10% (n=6) of transplants, all
located under crevices of which 3% using the grid method and 7% using the polystyrene method.
Sediment cover affected 7% of all transplants. They were in an erected position using the epoxy putty
method and it did not affect their survival.
23
Figure 8. Detachment of C. rubrum transplants (expressed in percentage) from the beginning of the experiments to November
2021 for each transplantation method at Gallinara Island.
Figure 7. Survival (expressed in percentage) of C. rubrum transplants from the beginning of the experiments to November
2021 for each transplantation method at Gallinara Island. There is a total period of four years for transplants under
crevices and of three years and a half for transplants on rocks.
24
3.2.2 Branching difference of transplants
In total 39 transplants were taken into account for branching difference calculation: 12 from the
polystyrene method, 5 from the grid on rocks method, 13 from the grid under crevices method and 9
from the epoxy putty on rocks method. It revealed that most of the transplants lost branches or their
number of branches remained stable from the moment they were transplanted to the last survey they
were alive, independently of the transplantation method (Figures 9 and 10; Appendix Figure A).
Indeed, from the polystyrene method and grid on rocks method 50% and 60% of transplants lost
branches respectively. Fewer transplants lost branches using the grid under crevices method (46%)
and the epoxy putty method (44%). Transplants gained branches only using the polystyrene method
(17%) and the grid under crevices method (8%). All methods confounded, 56% of transplants lost
branches with an average of 35.8±21.1% of loss, 8% gained branches and 36% remained unchanged
(no loss nor gain). On average, transplants from the polystyrene method, grid on rocks method, grid
under crevices method and epoxy putty on rocks method have a branching difference of respectively
-19.5±30.2%, -10±10.6%, -16.2±30.1% and -13.4±18.6%. One transplant from the grid under crevices
method even lost 89% of its branches while others gained up to 22% of branches. Results of the
Kruskal-Wallis showed no significance (p-value=0.99), suggesting that there is no significant difference
between the different transplantation methods regarding the branching difference
Figure 9. Change in the number of branches (branching difference, in percentage) of C. rubrum transplants for each
transplantation method in Gallinara Island. The red cross represents the average. Boxes' width is relative to the number of
transplants.
25
3.2.3 Height growth of transplants
In total, only 13 transplants could be measured from the grid method: 10 under crevices and 3 on
rocks. Measurements were not very precise due to a poor scale bar, therefore the presence of a height
increase followed by a decrease of the same scale is not counted as a variation in height. In November
2021, transplants’ height decreased on average by 24% for the ones under crevices and by 1% for the
ones in an erected position (Figures 10 and 11; Appendix Figure A). Most of the transplants under
crevices (80%, n=8) decreased in size one year after transplantation and 20% (n=2) continued to
decrease after that. Only one transplant decreased in size (18%) after one year using the grid on rocks
method while the two others may have increased in size. Spearman’s correlation test results show a
very poor and non-significant correlation (p-value=0.4689, rho=0.024) between branching difference
and height growth (Appendix Figure B) but this test was only performed on 13 samples.
Figure 11. Height growth (expressed in percentage) of C. rubrum transplants using the grid method under crevices (left) and
on rock (right) from the beginning of the experiment until November 2021 with the average (red line) and standard
deviations. A growth stopping translates to a transplant loss.
Figure 10. Corallium rubrum transplanted using the grid method under a crevice. First day of the experiment with all their
branches and initial sizes (A), one year after transplantation with lost branches and decreased size (B) and the last survey
with one transplant covered by epibiosis (C).
Nov 2021
Jul 2018
Oct 2017
A
B
C
26
3.3 Transfer of colonies and settlers from shallow to deep waters
3.3.1 Survival and detachment of transplants
Survival rate of transplanted shallow colonies in deep waters is 82% (n=30) after one year and a half.
The 18% loss is exclusively due to detachment of transplants from the epoxy putty, no death was
observed. In the last survey in October 2019, 59% of transplants were affected by sediment cover, but
they all looked healthy with predominant polyps. Of survived transplants, 3% (n=1) was affected by
branching decrease by losing 12.5% of its branches. Otherwise, all other survived transplants did not
experience any branching difference.
3.3.2 Survival of shallow settlers and settlement of deep settlers
Three PVC tiles were identified from the survey's sampling (tile A, tile B and tile C) of which one picture
sample is missing in the first survey (tile C). Shallow and deep settlers could then not be identified in
tile C. Survival rate of shallow settlers after one year and a half in deep waters is 31% on tile A and
50% on tile B (Figure 12). The number of shallow settlers on tile B decreased by 50% after two months
and remained stable for the rest of the experiment, on the other hand, the number of shallow settlers
in tile A decreased continuously until October 2019. Tile A had 3.25 shallow settlers·dm-2 at the
beginning which decreased to 1 shallow settler·dm-2 by October 2019 (Figure 13). Tile B had a higher
survival rate of shallow settlers but had a smaller density of shallow settlers at the beginning (0.5
shallow settler·dm-2) that decreased by half by October 2019.
Larvae from deep C. rubrum colonies were observed to settle on both tiles during the spawning events
of 2018 and 2019 (Figure 13). In 2018, settlers appeared in June and September 2018 on both tiles,
while in 2019 settlers only appeared on tile A. Tile A had 2.25 deep settlers·dm-2 in June 2018 which
decreased to 0.75 deep settlers·dm-2 by October 2019. Tile B had 1 deep settler·dm-2 in June 2018
which decreased to 0.75 deep settlers·dm-2 by October 2019. Settlers from the 2018 cohort were lost
on tile A (22%) and B (75%). In October 2019, shallow settlers dominated tile A (57%) while they were
the least abundant on tile B (25%) that was dominated by deep settlers from the 2018 cohort (75%)
(see fig). The average settlement density of shallow and deep settlers are 1.28±1.14·dm-2 and
1.33±0.59·dm-2, respectively (from April 2018 to October 2019). Including tile C, the total average
settlement density of all settlers confounded is 1.98±1.52·dm-2, with tile A having the highest one
(3.63±1.14 settlers·dm-2).
27
Figure 12. Survival (expressed in percentage) of C. rubrum shallow settlers on PVC tiles from the beginning of the experiment
in deep water to October 2019 at Portofino MPA.
Figure 13. Settlement density (expressed in settlers·dm-2) of C. rubrum shallow and deep settlers from the beginning of the
experiment in deep water to October 2019 on each tile at Portofino MPA.
28
3.4 Scleraxis structure of apical parts
Different scleraxis structures were observed in Gallinara transplants fragments. The clean-cut caused
by the pinches is clearly identifiable (Figures 15A-B) and shows a regular pattern of sclerite-like
protuberances at the bottom of the fragment. The apical part of one fragment had a smoother pattern
with few sclerite-like protuberances (Figure 15F) compared to the Portofino fragment from 1960
(Figure 14B), suggesting an alteration occurred changing the scleraxis structure. The apical fragment
pictured in figure 15G shows two straight structures similar to a cut, suggesting a loss of branches. The
straight structure on the side has an uncommon swelling (Figure 15H) with a regular pattern of
sclerite-like protuberances (Figure 15I) suggesting a regeneration process.
The fragment detaching itself from the colony (Portofino, 25m depth) has a sub-apical part
significantly different from the clean-cut one (Figure 15J) with the inner part retracting itself (Figure
15K) as a dissolution process. It also shows a smoother and irregular pattern of sclerite-like
protuberances (Figure 15L). This structure corresponds to the fragmentation process observed
underwater leading to full detachment of the apical part and thus a branch loss.
A fragmentation process reconstruction can be hypothesised with this scleraxis analysis: the
dissolution process leading to branch detachment (Figures 15J-L) from the colony left with a straight
cut (Figure 15G apical part) that later on will start a regeneration process (Figures 15H-I).
.
Figure 14. Scleraxis of 60 years old C. rubrum apical fragment from Portofino seen under a microscope (A). Apical scleraxis
structure details under a SEM (B).
A
B
29
I
Figure 15. Scleraxis of C. rubrum apical fragments from transplanted colonies at Gallinara Island (A-I) and from Portofino
MPA at 25 m depth (J-L.) Scleraxis seen under a microscope (A, D, G, J). Closer look of interested parts under a SEM (B, E, H,
K). Scleraxis structure details of the interested part (C, F, I, L). Clean cut done by metal pinches (A-C). Apical part with a
smooth pattern (F). Apical and side branches previously fragmented (G) undergoing a regeneration process (H-I). Bottom
part of the apical fragment with a dissolution process (J-L).
A
B
C
D
E
F
G
H
I
J
K
x0.8
L
x0.8
x0.8
x1.25
100μm
100μm
100μm
v
E
30
4. Discussion
The short review on methodologies to transplant red coral colonies and the description of original
pilot activities to test different approaches provide useful suggestions for future Corallium rubrum
restoration strategies. The peculiarity of red coral with respect to other gorgonians is its hard tree-like
skeleton, allowing to handle easily the colony during transplant. This has generally addressed previous
experience, generally adopting putty or structures holding colonies (e.g., pinches in Monte Carlo
artificial caves).
In terms of survival, we can affirm that the current knowledge suggests that the best methods are
using a two-component epoxy putty as glue to attach transplants on coralligenous substrate in an
erected position (71.5% of survival after 2-4 years). The fact that loss of transplants was always due to
method failure or detachment highlights the resistance and adaptive abilities of shallow red coral
colonies previously introduced.
In terms of reproduction, it seems that the best results are those recorded under roofs with numerous
small colonies (0.1-0.15 colonies·dm-2) settling on the roof of artificial caves (e.g. Monte Carlo artificial
caves) and numerous juveniles and colonies (2.25±1.70 juveniles·dm-2, 0.9±0.3 colonies·dm-2) settling
on PVC tiles in natural caves (e.g., Colombara cave and Marseilles).
This thesis presents the first in situ experiment of transplanting C. rubrum under crevices with two
promising techniques to maintain the fragments: polystyrene and PVC grids. After four years, they
showed a similar survival rate (30% and 32%) but the polystyrene method seemed less effective at the
beginning with transplant detachment recorded in the first week and months. The disadvantage of
the grid method is the risk of grid detachment from the substrate, resulting in a high sudden transplant
loss (48%). While detachment was the main cause of loss and occurred in both methods, it was earlier
but slower with the polystyrene method and later but suddenly with the grid method. The grid method
seems therefore more reliable to transplant C. rubrum under crevices.
A new technique is introduced to attach transplants on coralligenous substrate in an erected position
by using a PVC grid as an extra holding material. Even though it showed the best survival rate (60%)
of all techniques and the lowest detachment rate (40%), the loss was also caused by grid detachment.
This method failure goes against the initial intention of the technique to avoid transplant loss. In total,
from under crevices and on rocks, two grids fell out of five originally. It is evident that for better results,
grid fixation on the substrate should be improved in further experiments and thus improve the survival
of transplants and technique effectiveness.
31
The survival rates of the presented techniques are similar to the ones from transplantation
experiments carried out with Mediterranean gorgonian species (30%-98% of survival) (Linares et al.
2008; Fava et al. 2009; Montero-Serra et al. 2018; Montseny et al. 2019; Casoli et al. 2021). However,
they are lower than the average reported for previous C. rubrum experiments (71.5%) all done in an
erected position, suggesting the inclination of the substrate can strongly affect survival of
transplants. Additionally, one has to take into account that the sample size used in each technique,
especially for the grid on rocks method (n=5), were considerably smaller compared to previous C.
rubrum transplantation experiments (average sample size of 141.5±67.3). Therefore, we strongly
recommend increasing sample size, especially for promising techniques using PVC grids, in order to
obtain more accurate results.
The loss of branches and decrease in height observed at the beginning of the experiments,
independently of the technique used, suggest an adaptive behavior from C. rubrum to cope with new
environmental conditions and respond to stress. These observations alone support the hypothesis of
an autotomy procedure of C. rubrum branches during the transplantation experiments. The scleraxis
structure analysis reveals a fragmentation like-process in C. rubrum apical parts, observed in situ in
Portofino MPA (25 m) and deduced by SEM observations in transplanted colonies of Gallinara Island.
The structures seen under SEM were not similar to what could be found in today’s literature (Grillo et
al. 1993; Vielzeuf et al. 2008; Chaabane et al. 2019) thus further research is necessary to study them
in order to fully understand the calcification process behind them. To our knowledge, this study
reveals the first microscopic observation of the autotomy procedure of branches first reported by
Russo et al. in 1999. The lack of correlation between the branching difference and variations in height
growth may be due to the small sample size, or it could reveal that the branches lost were not only
the apical branch but also side branches, which was seen under the SEM.
Despite the genetic differences between shallow and deep red coral populations, shallow colonies
also seem able to survive in deeper environments according to the successful transfer experiment
(82% of survival) with no sign of suffering: on the opposite of transplantations in shallow waters,
transplants did not lose branches nor were affected by mortality. This thesis also introduces the fact
that shallow settlers can survive at 70 m depth after one year and a half. Those results date to October
2019, thus a new field survey should be conducted to evaluate the state of transplants colonies and
the survival/growth of shallow and deep settlers. As only two tiles were identified results should only
be considered as an indication, and improvement of photographic sample ID is required for further
experiments.
32
While previous larval enhancement experiments focused on shallow environments, this study
presents the ability of C. rubrum deep colonies larvae to settle on tiles for two consecutive spawning
seasons despite the fact of bryozoans and turf algae colonizing the surface. The deep settlement
density observed (1.33±0.59 settlers.dm-2) was smaller than recruitment densities reported for
shallow populations, probably explained by the highly fragmented seascape of deep red coral colonies
(Cau et al. 2016) and the limited connectivity in this species (Constantini et al. 2016). Substrate
suitability might be a limiting factor for deep larval settlement (Cau et al. 2016) but the PVC tiles used
seem to be suitable.
5. Conclusion
Historical data on red coral fishing activity can offer a good picture of the distribution of red coral in
the past, suggesting where restoration actions should be prioritized. The data on survival rate reported
here suggest the geomorphology of the cliff is an important variable to be considered when
restoration plans are designed, and the inclination of the substrate can strongly affect both the
survival of transplants and the eventual pattern of recruitment. Corallium rubrum is a very resistant
and adaptive species as shown with the autotomy procedure and the low mortality rate of transplants
in the shallow transplantation techniques reported here. These techniques are waiting to be further
improved and assessed to reach a higher percentage of survivors and guarantee an effective
restoration, with reproductive colonies and the recruitment of larvae coming from transplants. With
deeper populations being harvested, the successful transfer methods reported here offers a way to
populate them before banks get completely depleted. Finally, this study offers restoration tools for C.
rubrum currently lacking in today’s literature;
33
Acknowledgements
I am extremely thankful to my promotor Prof. Dr. Carlo Cerrano and my supervisor PhD student
Torcuato Pulido Mantas to have supported me in the numerous change of thesis plans due to the
COVID-19 pandemic and giving me this final opportunity. I am grateful for Prof. Dr. Carlo Cerrano
knowledge that he gently shared with me and for Torcuato Pulido Mantas input throughout my thesis.
I gratefully recognize the help of the Dipartimento di Scienze della Vita e dell’Ambiente from
Università Politecnica delle Marche for their welcoming atmosphere and giving me the necessary
equipment to accomplish my experiments. I would like to give a special thanks to the PhD student
Camila Roveta for her guidance and help in laboratory experiments.
Thank you to the staff of the Marine Protected Area of Portofino for authorization of collecting data
and to Portofino Divers Diving Evolution who made the surveys possible by providing the logistics.
Thank you to my family for their support and belief in me. Most special thanks to my partner Jan
Bierwirth for being by my side during the last completed year and giving moral support when it was
most needed.
34
Appendix
Table A. List of articles considered to summarize C. rubrum transplantation experiments
Author
Location
Technique
Depth
(m)
Period
length
Substrate
type
Survival
rate
Detachmen
t rate
Mortality
Number of
colonies
Weinberg 1979
Banyuls-sur-Mer
Hard PVC-tube with 2 incisions
+ screws to hold the fragment
fixed on cement blocks
10
few
weeks
Photophilo
us algae
0%
0%
100%
Bianconi et al.
1988
Scandola (Corsica)
Fixed on panels with metal
wire
36-39
Coralligeno
us
0%
0% (whole
panel fell)
100%
Giacomelli et al.
1988
Naples Zoologic
station
Hanging colonies facing down,
tied with a copper wire
Aquarium
Used a
few
colonies
Arosio et al.
1988
Alghero
(Sardegna)
Resin and stainless steel
tweezers
Coralligeno
us
Cattaneo-Vietti
et al. 1990
Montecarlo
Marine Reserve
(i) Fixed with bolts to
polypropylene panels (ii) held
with plastic tweezers (iii) glued
into porphyry bar wholes with
Devcon resin
27/35
2 years
Artificial
cement
cave
40%
60%
0%
Pais et al. 1992
Alghero
(Sardegna)
Quick-settling cement as glue
in holes on small tiles.
25
Small
concrete
pipe with
metal base
100%
2 colonies
0
Chessa et al.
1997
Alghero
(Sardegna)
Small boards with ready-to-set
concrete
Cement
tube
100%
0
0
Cerrano et al.
1997
Gallinara island
Oily putty normally used for
glass panes applied in the
crevices as glue
20-24
Coralligeno
us
0%
100%
0%
35
Cerrano et al.
1997
Gallinara island
Two-component epoxy putty
as glue with 3-4h curring
20-24
1
month
Coralligeno
us
100%
0%
0%
50
Cerrano et al.
2000
Portofino, Punta
del Faro
Two-component epoxy putty
35
3 years
Coralligeno
us
10%
100
Cerrano et al.
2000
Portofino,
Mohawk Deer
wreck
Two-component epoxy putty
34
3 years
Metal
sheets of
wreck
0%
100
Cerrano et al.
2000
Gallinara island
Two-component epoxy putty
24
3 years
Coralligeno
us
50%
300
Cerrano et al.
2000
Gallinara island,
Umberto I wreck
Two-component epoxy putty
40-50
3 years
Metal
sheets of
wreck
0%
140
Cerrano et al.
2000
Sorrentina
peninsula, Scoglio
del Vervece
Two-component epoxy putty
45
3 years
Coralligeno
us with A.
cavernicola
80%
100
Cerrano et al.
2000
Sorrentina
peninsula, Punta
Campanella
Two-component epoxy putty
38
3 years
Biocenosis
of A.
cavernicola
80%
100
35
and E.
singularis
Cerrano et al.
2000
Sorrentina
peninsula, Secca
della Vetara
Two-component epoxy putty
38
3 years
Biocenosis
80%
100
Ledoux et al.
2015
Riou Island and
Palazzu Island
Disks with 8 holes (1 hole=1
colony), no putty used.
20/40
few
month
s
Plates
made of
PVC disks
100%
0%
0%
192
Montero-Serra
et al. 2018
Parc Natural del
Montgri, Illes
Medes i Baix Ter
Two-component epoxy putty
15-17
4 years
Coralligeno
us
99.10%
300
Table B. List of articles considered to summarize C. rubrum larval enhancement experiments on tiles
Author
Location
Technique
Depth
(m)
Density (settlers·dm-2)
Number of
settlers
Period
length
Cerrano et
al. 2000
Punta del Faro and
Colombara cave, Portofino
(Italy)
10 fiber cement panels fixed on vertical
and sub-horizontal walls
Vertical: 1.6 (Punta del Faro); 0
(Colombara) / Sub-horizontal: 5
(Puntal del Faro); 11.7
(Colombara)
2 years
Garrabou
et al. 2002
Marseilles (France)
12 Urgonian limestone (same geological
nature as the local coast) panels attached
together within a frame roped off to the
lateral wall of the cave
27
0.9 ± 0.3 colonies
36
(colonies)
21 years
Bramanti et
al. 2005
Calafuria coast (Italy)
20 white marble tiles fixed with a central
steel screw onto the vault of crevices
25/35
19.12±4.97 (25m); 9.75±2.87
(35m)
388
4 years
Bramanti et
al. 2007
Calafuria, Elba MPA and
Medes Islets MPA (Spain)
54 white marble tiles fixed via a central
Fisher’s screw to the substrate onto the
vaults of crevices
25-35
Calafuria 2.77±3.04; Medes
1.6±1.96; Elba 1.1±1.4
138
1 year
Benedetti
et al. 2011
Calafuria coast (Italy)
3 CaCO3 substrata (lithogenic CaCO3
(marble tiles), electro-accreted CaCO3 in
the absence and in the presence of
cathodic currents) fixed on the vault of
crevices with central Fisher’s screws
35
3±2.5 (marble tiles); 2.7±1
(electro-accreted CaCO3 plates
without cathodic current);
0.6±0.4 (electro-accreted CaCO3
plates with cathodic current)
1 year
Costantini
et al. 2018
Colombara cave, Portofino
(Italy)
16 white PVC tiles drilled in the centre
fixed inside the cave by steel screws
34-39
8.69±5.96 (recruits); 2.25±1.70
(juveniles)
372
2 years
36
b
Oct 2017
Jul 2018
Nov 2021
Oct 2017
Oct 2017
Nov 2021
Nov 2021
Sep 2021
Jul 2018
Sep 2018
Aug 2017
Nov 2017
Figure A. Corallium rubrum transplants in Gallinara Island with branch loss (A-C, G-H, J-L) and decrease in height (A-C, D-F, G-I, J-L) through time.
Grid under crevices method (A-I). Polystyrene under crevices method (J-L)
A
B
C
F
E
D
G
H
I
J
K
L
37
Figure B. Correlation between the branching difference and height growth of measured transplants (n=13) using the grid
method.
38
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The assessment of effective and affordable restoration interventions is pivotal to developing new tools to mitigate habitat loss and enhance natural recovery. Gorgonians create important three-dimensional habitats in the Mediterranean Sea providing several ecosystem services associated with coralligenous reefs. Transplantations of the octocorals Eunicella cavolini, E. singularis, and Paramuricea clavata were carried out at the site impacted by the wreck of the Costa Concordia in 2012. A total of 135 by-caught gorgonians, caught in the gears of local artisanal fishermen or found lying on the seabed by SCUBA divers, were transplanted on impacted coralligenous reefs between 20 and 35 m depth and monitored for 2.5 years. A high survival rate (82.1%) was recorded, with main losses attributable to the detachment of the organisms from the substrate rather than death of the colonies. Eunicella cavolini transplanted colonies and natural colonies used as controls were monitored and showed similar, and seasonally influenced, growth and healing rates. Epibiosis and necrosis events were reported in both transplanted and natural colonies during summer, highlighting the sensitivity of the species to thermal stress. The present study emphasizes the importance of a management framework as a stepping-stone to achieve effective restoration outcomes, including the removal of pressures that caused changes in natural communities and the participation of local stakeholders. The effectiveness of the methods and procedures proposed in this work allowed the restoration activities to continue at a larger scale during summer and autumn 2020. This article is protected by copyright. All rights reserved.
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Background. Larval settlement and intra-specific interactions during the recruitment phase are crucial in determining the distribution and density of sessile marine popu- lations. Marine caves are confined and stable habitats. As such, they provide a natural laboratory to study the settlement and recruitment processes in sessile invertebrates, including the valuable Mediterranean red coral Corallium rubrum. In the present study, the spatial and temporal variability of red coral settlers in an underwater cave was investigated by demographic and genetic approaches. Methods. Sixteen PVC tiles were positioned on the walls and ceiling of the Colombara Cave, Ligurian Sea, and recovered after twenty months. A total of 372 individuals of red coral belonging to two different reproductive events were recorded. Basal diameter, height, and number of polyps were measured, and seven microsatellites loci were used to evaluate the genetic relationships among individuals and the genetic structure. Results. Significant differences in the colonization rate were observed both between the two temporal cohorts and between ceiling and walls. No genetic structuring was observed between cohorts. Overall, high levels of relatedness among individuals were found. Conclusion. The results show that C. rubrum individuals on tiles are highly related at very small spatial scales, suggesting that nearby recruits are likely to be sibs. Self- recruitment and the synchronous settlement of clouds of larvae could be possible explanations for the observed pattern.
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The behaviour of Mediterranean octocoral planulae was studied in light-dark situations and in a light gradient. Larvae of Eunicella singularis (Esper, 1794) reacted photopositively but it is uncertain which mechanism (klinotaxis or klinokinesis) determines this property. The blind larvae probably possess a dermal light sense, but it cannot be excluded that the yolk contains photosensitive carotenoids while the symbiotic zooxanthellae may also play a role. The photopositive behaviour of planulae of this species explains some aspects of the distributional ecology of adult colonies. It was also found that for the induction of settlement and metamorphosis the chemical properties of a given substratum seem to be far more important than its roughness. Larvae of Corallium rubrum (Linnaeus, 1758) are geonegative and indifferent to light. This latter fact is surprising, since in nature the colonies are exclusively found in dark places. It is supposed, therefore, that tolerance of the colonies rather than larval choice determines light-dependent zonation of this species in nature.