Global knowledge
The searches yielded 514 results of which 508 were classified as research articles and six were reviews (full reference list available as underlying data (Bertolini & Pastres, 2021)). The first study was dated 1926, from which a few articles per year were produced until the 1960s, when the number started to increase to reach 35 articles in the year 2020. The number of publications related to restoration started to appear in the late 1990s and increased in the last five years, whereas research relating to aquaculture was emerging in the late 1970s, and while it followed the increasing trend, the overall output was generally lower (Figure 1).
Figure 1. Clustering of keywords.
Topic dendrogram generated by conceptual Structure, with the main words characterising each cluster.
The most prominent keywords found (N occurrences, %tot) were: Bonamia ostreae (52, 10%), Crassostrea gigas (28, 5.4 %), Restoration (21, 4%), Bivalve (16, 3%), Aquaculture (14, 2.7 %), growth (14, 2.7%), flow cytometry (12, 2.3%), temperature (12, 2.3 %), haemocytes (11, 2.1%), bonamiosis (10, 1.9%). A first interpretation of this result therefore is that infection appears as a highly studied aspect, with at least 13% of the studies concerned with infection from Bonamia. The clustering method used only 156 (30%) papers with common keyword associations, meaning that the remaining 70% of papers did not share important (appearing at least 10 times) terms in their keywords. Clusters are shown in the dendrogram in Figure 2. Words from subclusters are reported in Table 1.
Figure 2. Number of publications per year.
Main plot (full dots): total number of publications by year; top inset (stars): number of publications related to restoration by year; bottom inset (triangles): number of publications related to aquaculture by year.
Table 1. Subcluster characterization.
Words in title, keywords and abstract characterizing each sub cluster.
| Cluster | Subcluster | Words |
|---|
| 1 | N/A | Restoration, invertebrates |
| 2 | 1 | Biochemical, bonamia, conditioning, culture, development, effects,
growth, implication, larval, rate, restoration, survival, temperature |
| 2 | Crassostrea, gigas, magallana, native, pacific, species |
| 3 | Adriatic, bay, larvae, sea |
| 3 | 1 | Bonamia, detection, haemocytes, parasite, resistance, vitro |
| 2 | Haemocyte, haemolymph, infection, protozoan, stocks |
| 3 | Bonamiosis, Crassostrea, gigas, response |
Cluster one (green) had eight articles that dealt specifically with restoration. Sub-clustering was not possible due to the small number of papers Many aspects fell into this cluster: from the need of having high enough densities for successful reproduction (Eagling et al., 2018), and the seed collection stage (Colsoul et al., 2020; Rodriguez-Perez et al., 2020; van den Brink et al., 2020) to the suggestion that soft interventions such as protecting areas with a gravelly seabed may be a way to aid a natural come back in areas were a remaining natural population may be present even if in few numbers (Kerckhof et al. (2018)). The need to consider infection in restoration procedures was also part of this cluster (Sas et al., 2020). Ecosystem effects of restoration such as the proper quantification of carbon deposition (Lee et al., 2020) and the missing questions that must be answered for the integration of policy and practice (Zu Ermgassen et al., 2020).
Cluster two (blue) had 93 articles. Title sub-clustering identified three subclusters: subcluster 1 papers related mostly to growth and larval development, stock, reproduction, settlement, the effects of temperature and food. Restoration and diseases also appeared as words in this cluster. Subcluster 2 papers were on comparisons or interactions between C. gigas and O. edulis regarding species distribution, biomarkers, biochemical and genetic assays, but also epibionts. A third subcluster was formed by a single paper on the seasonal distribution of larvae in the Adriatic Sea.
Cluster three (red) had 55 articles. Title sub-clustering identified three subclusters: subcluster 1 included papers on infection (Bonamiae), immunological activity and selection; subcluster 2 comprised papers on haemocyte parameters from different brood stocks in different geographic areas; and subcluster 3 papers were on the genetics of infections.
This analysis also gives some insights into the focus of the research concerning Ostrea edulis: the most numerous clusters contained papers mostly concerning the ecology of the species, while the second major cluster was formed by studies on infection and disease. Some interesting patterns arose on the main issues that may be considered by both restoration and aquaculture of this species. Infection, particular bonamiosis, may be an obstacle to both activities, and it is important to acknowledge that many studies are present including a comprehensive review (Sas et al., 2020). Primary subjects of Bonamia publications were: presence and transmission (22), resistance (19) methodologies of detection (12), responses and impacts (11), environmental variables (2). However, despite the high number of papers, both (Sas et al., 2020) and (Holbrook et al., 2021) underline a necessity to understand better the environmental variables that will be responsible for the infection and the mechanisms of resistance.
In terms of this automated keyword association analysis, there appeared to be a few studies concerned solely with restoration. On the other hand, searching for restoration in keywords and titles manually yielded 35 articles, spanning from 1999 to 2021 (Figure 2). Geographically, studies were primarily from Atlantic and North Sea regions (France, Germany, Netherlands, UK, Figure 3). Out of these, 12 (35%, 1999–2020) are concerned with ecological understanding, in particular related to site selection and conditions for growth, 10 (31%, 2018–2021) were related to settlement and seed production, four (12.5%, 2018–2020) regarded policy, three (9%, 2016–2019) were concerned with methodology for restoration, three (9%, 2018–2020) touched on the benefits of restoration, two (6%, 2020–2021) dealt with infection in restored oysters and only one (3%, 2010) dealt with genetic diversity.
Figure 3. Annotated map representing countries where restoration (R) or aquaculture (A) studies are from.
Both the automatic clustering and manual search highlight how the ecological requirements that may be necessary to obtain a thriving and healthy population, thus towards ‘successful’ restorative aquaculture, are already widely studied. The restoration papers dealing with ecological understanding, for example, presented some agreements with regards to the value of the main environmental parameters necessary for success, as summed up in Table 2.
Table 2. Requirements for successful restoration.
Environmental
parameter | Optimal value | References |
|---|
| Current speed | 0.25–0.3 m/s | Kamermans et al., 2018; Merk et al., 2020; Pogoda et al., 2020 |
| Bottom shear stress | <0.3–0.4 N/m2 | Bennema et al., 2020; Pogoda et al., 2020 |
| Sediment type | coarse grain size or presence of
shell and stones for settlement | Allison et al., 2020; Christianen et al., 2018; Kamermans et al., 2018; Pogoda et al., 2020 |
| elevated cultch | Sawusdee et al., 2015
(as seen for other species Marshall et al., 1999; Wesson et al., 1999) |
| Water temperature | 7°C minimum for growth and
gonad development | Maathuis et al., 2020; Merk et al., 2020 |
| Oxygen | No agreement | |
| Chlorophyll | No agreement | |
Searching for aquaculture in keywords and titles manually yielded 21 articles, spanning from 1977 to 2020 (Figure 2). Geographically studies spanned both Atlantic and Mediterranean European regions (Croatia, France, Germany, Italy, Netherlands, UK, Figure 3), but there were also two studies concerning aquaculture of this species from the USA (Burrell, 1983; Mann & Ryther, 1977). Of the two largest subgroups of studies, one dealt with the practicalities of seed production, including selective breeding (6, 28.5%), and the other with growth and biochemical composition of the marketable oyster product (5, 24%). There were also studies concerned with ecological conditions at the production site (2, 9.5%), with interactions with C. gigas (2, 9.5%), with infections (2, 9.5%) and with effects on the environment (2, 9.5%). Single studies were also done on history (1, 5%) and farm management from the human perspective (1, 5%).
Despite their different endpoints, in order to reach their goals both aquaculture and restoration must obtain healthy adults. This results in research perspectives that can be shared between the two ‘branches’. One common theme that emerged between the two was seed harvesting or production, an issue affecting aquaculture that relies mostly on wild seed collection but also affects restoration programmes that rely on active ‘seeding’ of often large quantities of oysters. Within this theme, two papers (Colsoul et al., 2021; van den Brink et al., 2020) appeared in both searches. van den Brink et al. (2020) deals with the identification of the optimisation of collection, both in terms of collector types and methodology (e.g., timing), showing how ‘natural’ substrates (shell) would be optimal but raising questions related to the ‘economic viability’ of using this method for aquaculture purposes, which usually employs artificial collectors that simplify the process of detachment for the second phase of cultivation. Colsoul et al. (2021) provide a comprehensive review of seed production research in general, starting from the general biology of the species, identifying the stressors, and then looking at the history of production technologies, going into detail on seed production in polls, ponds and hatcheries. The review ends with a series of research gaps on the issue, such as the need to address the effects of climate change on reproductive patterns, something that is starting to be investigated in other bivalve species, e.g. mussels (Oliveira et al., 2021), but was already identified as a potential cause of O. edulis seed scarcity in 2015 (Burioli et al., 2015). This shows that an emerging field of ‘restorative aquaculture’ would need to address the issue of seed production, whether in situ or through hatcheries, ensuring enough seed can be collected or produced to ensure both economic viability and reefs creation/maintenance.
Historical and local knowledge
With regards to oyster knowledge in the northern Adriatic Sea, multiple sources were found spanning the end of the 19th and beginning of 20th century. The most notable were two reports on the status of oyster culture in both the southern (Molin, 1863) and northern (Molin, 1864) parts of the Venice lagoon, a book on oyster and mussel culture (Carazzi, 1893), and a thorough account of edible molluscs in the Venice lagoon with a whole chapter on oysters (Ninni, 1904). More recent (end of the 20th century) papers investigating settlement and culturing were also found (Pellizzato & Da Ros, 1985; Pellizzato & Renzoni, 1986). Many of these examples already mention failed attempts, in particular related to obtaining successful reproduction (“a mistake in which many who attempted cultivating oyster fell into was to believe that to have successful spat would be enough to have some seawater, some adult oysters as mothers and some tiles to serve as collectors” chapter XI (Carazzi, 1893)). In the two reports from the 1860s, the ‘substrate’ limitation driving oyster reef self-sustainment was highlighted, and the dredging of hard material from the bottom of canals was pinpointed as one of the leading causes of the dramatic oyster loss observed in the lagoon. It was suggested that adding cleaned oyster shells could bring natural populations back, leading to the formation of ‘oyster parks’ (Molin, 1863; Molin, 1864). The importance of location choice, collector specificity and timing, substratum type and environmental variables for the first stage of cultivation (seed harvesting) were already recognised as important (Carazzi, 1893), together with the need for oyster culture to rely on trials and ‘naturalists’ advice (Molin, 1863). The location of settlement, aside from having the right environmental conditions (for example a temperature warm enough to have sufficient spawning, even up to 28–30°C, but not higher to avoid mortality), would need to be close by to the location of culturing (at least for the first culturing phase, up to 3–4 cm) to avoid stressing the young oysters. The position of the collectors within the location was also already found to be an important issue: larvae were found to settle closer to the seabed, and for this reason, if collectors are on the seabed, it is important to ensure the sediment is neither too muddy to avoid sinking nor too sandy (indicative of too strong currents). The timing of collectors’ placement was also already identified in these early texts as an essential aspect that could be as important as the materials, as both too early and too late can have negative effects, either due to fouling by other organisms (if placed out too early) or due to missing the settlement period (when placing too late).
