2.1. Colonization of Artificial Substrata
Biofouling is a complex process that involves colonization by microfouling organisms, such as viruses, bacteria, cyanobacteria, fungi, protozoa and microalgae, and larger macrofouling organisms, including macroinvertebrates and macroalgae [13
]. Macrofouling comprises calcareous hard-fouling organisms such as acorn barnacles, mussels and tubeworms and soft-fouling organisms such as non-calcareous algae, sponges, anemones, tunicates and hydroids.
The colonization process is often broadly described as a succession of four main stages, as shown in Figure 1
Within minutes to hours of submersion, the substrata adsorb a biochemical conditioning biofilm, consisting of organic material such as glycoproteins, proteoglycans and polysaccharides naturally dissolved in the seawater.
Within hours, primary colonizers, assemblages of unicellular organisms that secrete extracellular polymeric substances (EPS) adhere to the substrata. Together, the microorganisms and EPS facilitate the settlement of macrofoulers.
Within days to weeks, secondary colonizers consisting of sessile macrofoulers, including soft- and hard-foulers, develop and overgrow the microfouling. As they grow and age, macrofoulers provide “micro-habitats” that attract further settlements.
Within weeks to months, the substrata are fouled by tertiary colonizers which typically reside within the sessile biofouling. The biofouling communities reach maturity within a few years, accompanied by an increase in species diversity and richness. The communities are characterized by a variety of sessile and mobile benthic and epibenthic organisms.
While this classic “successional” model may represent major patterns of biofouling development, it oversimplifies the colonization process as implying causality from stage to stage. It is now widely accepted that colonization follows a more dynamic and “probabilistic” model (Figure 1
b), in which the absence of a stage does not impede the occurrence of another stage. For example, some acorn barnacle and bryozoan species may settle on a substratum without the presence of a conditioning biofilm [18
]. Colonization is thus greatly dependent on the type and number of organisms, whose settlement is independent of one another, that could attach to or colonize the substratum [16
]. In the absence of a substratum, foulants may aggregate and form marine snow [16
], which remains in seawater and may eventually attach to a substratum. Living organisms such as invertebrate larvae and algal spores trapped in the marine snow grow after attachment [20
2.2. Factors Influencing Marine Biofouling
The composition of biofouling communities varies greatly geographically, seasonally and locally across depths or in different levels of wave exposure and is influenced by numerous abiotic and biotic factors [13
]. The abiotic factors include the physical-chemical characteristics of seawater, such as temperature, pH, dissolved oxygen and organic matter content. In addition to those factors, abiotic factors include hydrodynamic conditions such as current velocity, wave exposure, distance to shore and depth. Substratum features such as the material composition (for example, metal vs. plastic), color, roughness, period of submersion and motion (for example, free moving equipment such as tidal turbines vs. static structures such as foundations) also influence settlement and growth [21
]. Among biotic factors, the biology of the different organisms will dictate how likely a settlement is on a submerged substratum. This, in turn, depends on many species–specific interactions and can differ greatly from species to species in different locations. In addition, chemical cues released in response to competition, reproduction, grazing and predation also play a big role in the settlement and surface recruitment of different organisms [24
]. Many of the factors are interrelated, and all are directly or indirectly affected by seasonality and location.
While the biofouling process evidently is complex and highly dependent on physical, geographical, and biological parameters, the current paper will focus on a selection of important abiotic factors.
2.2.1. Seawater Temperature
Seawater temperature is related to latitude and seasonality and is a major geographical determinant of the composition of marine communities, including biofouling composition, influencing the spawning period, settlement, growth and reproduction of organisms [27
]. Generally, biofouling growth rate increases with temperature and therefore less biofouling is expected closer to Polar areas owing to the lower temperatures (<5 °C). In those regions, biofouling occurs typically during mid-summer when temperatures are higher. In contrast, in tropical to sub-tropical locations, biofouling is generally more intense since the warmer temperatures (>20 °C) allow continuous reproduction throughout the year, enabling an increased growth rate of the biofouling organisms. In temperate areas, with mild temperatures (5–20 °C), biofouling will occur throughout the year and show strong seasonality, with most spawning and growth occurring from spring (beginning of April) to early autumn (end of October) [21
]. The temperature of the substrate where organisms grow have significantly less influence on the growth [29
2.2.2. Depth and Light Availability
Depth and light availability greatly affect the composition and growth of biofouling organisms. Macrofoulers, especially photosynthetic organisms such as macroalgae, are usually more abundant in sections within the euphotic zone (0–40 m) [30
]. This zone is generally warmer, presents higher light levels and is rich in plankton, which serve as the main food resource for many non-photosynthetic organisms. As a consequence of a decreased light intensity with depth, within this zone, the biofouling growth and biomass generally decrease with depth [21
]. Despite the decrease in biofouling pressure with depth, the settlement of sessile, filter-feeding invertebrates such as acorn barnacles and mussels, which often constitute the bulk of macrofouling, occurs down to great depths [31
2.2.3. Currents and Distance to Shore
Both the composition and extent of biofouling on a colonizable substratum are affected by currents and the distance from shore [29
]. Many organisms such as mussels, barnacles and tubeworms benefit from currents as they feed on particles suspended in the water or on nutrients dissolved in the water [15
]. The motile larvae of many invertebrates and the spores of algae are carried offshore by currents and, the closer is the substratum to the shore, the higher is the probability of colonization success, especially of fixed structures such as platforms [29
]. The impact of currents and water flow on biofouling communities will depend on the velocities and shear forces that are generated near the substratum [32
]. For example, while sessile filter-feeding organisms may benefit from high flows in terms of receiving particles as food resource, strong currents may dislodge organisms from the substratum. To cope with dislodgement when in the adult form, many sessile organisms such as barnacles have developed sophisticated mechanisms for strong surface adhesion [33
]. On the other hand, lower flows may facilitate the settlement of larvae/spores of some organisms.
2.2.4. Material of Substrata
The different materials used as artificial substrata will dictate their reactivity and toxicity and, therefore, influence the biofouling susceptibility of the substrata. The physical-chemical properties of materials can affect the water chemistry and seawater–substratum interface chemistry, influencing the formation and nutrient composition of the macromolecular conditioning layer. These properties affect the bacteria present on the substratum, usually with greater diversity being associated with biologically and chemically inert substrata which are more stable, thus facilitating rapid macromolecular conditioning and subsequent biofilm formation [36
]. This, in turn, may affect macrofouling settlement and growth. It has been reported that aluminum, carbon steel and bronze are more susceptible to biofouling than some non-metallic substrata such as glass fiber, polyethylene, polyamide and rubber [1
]. Among metallic substrata, aluminum-based substrata appear to present much less biofouling compared to for example bronze- and Monel-based ones (Vinagre et al. 2019 unpublished data). However, the response of biofoulers to materials is not universal and different biofouling groups or different species within-group may display different responses to the same material depending on factors such as temperature and depth.
2.2.5. Topography and Wettability of Substrata
The topography of substrata influences the physical and environmental conditions offered to the organisms. Higher heterogeneity of the substratum will allow for different microhabitats by providing a larger surface area, which enables higher diversity and lower competition between species. The level of microtopography, roughness and texture may also influence the ability of organisms to adhere to that surface affecting, for example, biofilm accumulation and subsequently the biofouling extent [32
]. Many algae have non-motile spores with low or no selectivity for substratum and to those the microtopography is important in physically restraining the spores and allowing them to adhere. Moreover, settlement of many invertebrate larvae is affected by microtopography, acting as cues assisting larval site selection [4
]. Therefore, smoother surfaces are generally less susceptible to biofouling than rougher surfaces [39
The microtopography of a substratum affects its wettability, and this influences the adhesion of biofouling organisms as the wetting process determines the actual contact area and interaction force between the adhesive and the substratum. However, no unique relation can be established between the hydrodynamic characteristics of the surface and the adhesion strength of the organism. For example, while the adhesive strength of acorn barnacles seems to be greater on high wettability surfaces [18
], different species appear to settle at a higher rate on hydrophobic substrata (Balanus improvisus
) or hydrophilic substrata (B. amphitrite
2.2.6. Color of Substrata
The color of a substratum relates to the amount of energy reflected and absorbed by the substratum, as well as to the temperature of the substratum, which can be determinants of biofouling settlement [42
]. It has been shown that the color of a substratum exerts a greater influence on the early stages of biofouling and is thus mainly a factor to consider for equipment that are submersed for short periods. Larvae and spores of many organisms show a negative phototaxis and prefer darker and less reflective substrata during settlement [41
]. In addition, bacterial biofilms are affected by substratum color and could thus be important in dictating the subsequent biofoulers which may not be directly influenced by the substratum color [43
]. Over time (months-years), as the biofouling communities become more complex, differences between darker and lighter substrata should become negligible [45
2.4. Impact of Key Biofouling Groups to MRE Equipment
The impact of biofouling is most often associated with alterations of the hydrodynamic properties, structural mass and roughness of submersed devices/components leading to loss of integrity and of performance or functionality [79
]. A summary of each impact is presented below:
● Added weight to MRE equipment
Among the five biofouling groups mentioned above, mussels, barnacles and kelp are the most problematic with regards to added weight. Mussel assemblages rapidly add substantial weight to structures. For example, in one study offshore the Portuguese West coast, M. galloprovincialis
registered ~24 kg fresh weight m−2
on test panels submersed for 12 months at 5 m depth (Vinagre et al., 2019, unpublished data). In another study in the Mediterranean Sea, after a much longer period of equipment submersion (offshore gas platform piles submersed for ~17.5 years) assemblages of M. galloprovincialis
registered ~155 kg fresh weight m−2
near the surface [81
]. While not as heavy as mussels, barnacles and bryozoans may also add considerable weight to structures. For example, offshore the Portuguese West coast, the barnacle Perforatus perforatus
and the bryozoan cf. Bugula
sp. registered ~4–5 kg fresh weight m−2
on test panels submersed for 12 months, at depths of 10 and 5 m, respectively (Vinagre et al., 2019, unpublished data). Colonies of the bryozoan Schizoporella errata
from the Mediterranean Sea (on offshore gas platform piles submersed for ~17.5 years) have further been recorded to also reach ~5 kg fresh weight m−2
at a depth of 12 m [81
]. Kelp assemblages regularly amount to great weights in their natural environment (e.g., up to 40 kg of fresh weight m−2
]). However, since they are close to neutrally buoyant, to MRE equipment kelp mainly cause increased drag of the moving parts [82
● Added thickness/roughness to MRE equipment
Mussels, barnacles and, to lesser extent serpulids, bryozoans and kelp, further greatly increase the surface diameter/thickness and roughness of submersed devices and components leading to increased drag and reduced mobility of moving parts [82
]. Furthermore, it is possible that the increased surface diameter/thickness of components could damage other, more sensitive components such as sealings from hydraulic components.
● Corrosion in MRE equipment
As mentioned in the Introduction, corrosion of MRE equipment may be induced and/or accelerated by micro- and macrofouling organisms [7
]. Anaerobic marine microorganisms may induce MIC and macrofoulers may facilitate MIC initiated by those organisms growing under the macrofoulers in hypoxic/anoxic conditions. In addition, some macrofoulers may promote localized corrosion as they use chemicals to adhere to or perforate substrata [8
]. While each of the five biofouling groups addressed in the current paper are capable of strongly adhering to substrata to different degrees, barnacles and serpulids generally show the greatest adhesion strength [83
]. Of the two, barnacles are usually more difficult to remove from MRE equipment compared to serpulids, and they usually cause more severe implications [84
]. This is often because it is frequently not possible to entirely remove barnacles without scratching the surface as their cement remains adhered to the surface upon removal, and this scratching may expose the surface to marine water and induce accelerated corrosion. The adhesion strength of barnacles specifically can be reduced using silicone coatings to which their attachment is weaker [85
]. Kelp, mussels and bryozoans generally show weaker adhesion strength and are easier to remove during maintenance. However, the forces generated on these settled assemblies of organisms by currents and waves may cause abrasion of the devices/components due to their great weight or volume and accelerate corrosion as a consequence.
Maintenance plans for MRE projects are of paramount importance as maintenance is a very costly process that may account for up to almost a third of the operating costs for an MRE project [86
]. Maintenance such as repair and inspection activities of MRE structures are carried out in situ, frequently offshore, during the service life of the setup [87
]. Those activities require specific and expensive operational logistics such as vessels, professionals and equipment, and they further hinge on environmental conditions and weather. Since MRE equipment/structures are designed to optimally perform from 10 to 30 years, maintenance is especially relevant during mid to later stages of the operational lifespan, as current antifouling solutions may not be functional during the entire lifetime of the project [87
]. Furthermore, maintenance activities also lead to downtime, preventing energy production and consequently causing loss in revenue. Because of the variable nature of biofouling and of its impacts on MRE structures/equipment, the biofouling database could be of especial importance for players in the MRE sector allowing them to be more aware of site-specific biofouling and aiding them in defining adequate maintenance plans including nature and frequency of activities.
2.5. Biofouling Control
Biofouling control has evolved especially in the last decade and it is anticipated that it will continue to do so, in particular in response to the changing environment [89
]. Several extensive reviews have been published on the topic over the last 60 years (Table 1
Until recently, antifouling solutions mainly resided in the use of biocidal substances, mostly tributyltin (TBT) or copper-based [99
]. While TBT was very effective, its pronounced persistence in sediments and bioaccumulation combined with substantial evidence of its significant environmental impacts on numerous non-targeted marine species such as mollusks and fish led to its global ban in 2008. As an alternative to TBT, the use of copper/zinc and booster biocides (e.g., Irgarol 1051, SeaNine 211 and Diuron) in antifouling paints became more frequent. Although these compounds are considered less harmful to the environment than TBT, similar problems associated with their toxicity and accumulation in the marine environment from their use have been reported [46
]. These methodologies rely on the release of a biocidal or repelling compound to counter the settlement of organisms and the coating/paint in which those substances are incorporated need to be reapplied at regular intervals.
Having a coating where the organisms attach poorly is an alternative strategy and, to date, the majority of applied antifouling technologies rely on such fouling release-based coatings, which were extensively reviewed by Lejars et al. [5
]. This has led to the development of numerous biocide-free antifouling solutions, such as silicone-based foul release coatings (e.g., Intersleek 900) capable of acting against both micro- and macrofouling organisms due to their amphiphilic surface nature and hydrogel paints (e.g., Hempasil X3) that form a water-retaining polymeric network over the coated surface and make the fouling organisms perceive the coated surface more as a liquid rather than a solid surface [103
]. The fouling release coatings are efficient when employed under suitable conditions; however, the technology is optimized for moving objects and relies on the sheer forces induced from movement to remove the settled organisms [5
]. As such, many of the silicone-based technologies are not optimized for the ocean energy sector with its many slow-moving or stationary marine installations.
With the development and expansion of maritime sectors such as ocean energy and aquaculture, the antifouling industry has grown proportionally [88
]. Alternative antifouling technologies are therefore under constant development. While new technologies are being developed, they must adhere to the legislation applicable to antifoulants, namely The Biocidal Products Regulation (BPR, Regulation (EU) 528/2012) which governs the use of antifouling coatings and other products.
Creating coatings that are effective and repellent to settlement under stationary conditions is challenging and many different strategies are under development and consideration in addition to classic biocide and fouling release technologies. Some examples include mechanical cleaning, physical control by applying acoustics [102
], pressure or UV radiation [108
], electro-chemical treatment [109
], iodine vapor [110
] and the development of repellent micro- and nano-textures [111
]. Several of these approaches are inspired by how stationary marine organisms cope with the threat of being overgrown and colonized [112
]. Stationary and slow-moving marine organisms regularly employ either a physical or a chemical defense to prevent being overgrown and colonized by marine micro- and macroorganisms and many of these approaches are being investigated [114
]. Biomimicry of natural repelling topographies such as shark skin, crab shells and plant leaves are thus under investigation [117
]. Numerous antifouling natural products exert their repelling effect in a non-toxic reversible manner, and being able to mimic nature would potentially allow for environmentally-friendly coating technologies [114
]. A challenge here lies in the economical production of large amounts of these compounds synthetically to meet demand, and structural simplification is one route to lower production costs [114
]. In addition, reducing the release to a minimum or employing contact-active biocides embedded in a soft coating would lower the environmental burden [10
For the marine energy sector, it is crucial that the antifouling is efficient, long acting and economical as these stationary structures are deployed for many years and repeated maintenance represents high costs for the sector [87
]. Several types of structures may not need total protection from settling organisms, while, for other more delicate, moving parts, it is crucial. In addition, given the spread in devices employed, it is unlikely that single solutions would be applicable to the entire sector [121
2.6. Artificial Reef Effect: Non-Native Species and Regulatory Framework
Any artificial structure deliberately placed in marine conditions will act as an artificial reef, attracting marine organisms and mimicking the functions of natural reefs [122
]. Offshore structures, although serving a different purpose, can be regarded as artificial reefs creating new surfaces on which the organisms attach, settle and grow [123
]. Therefore, offshore structures may act as promoters of ecosystem diversity and function and often present communities more diverse and abundant than those in the surroundings, including natural reefs and soft substratum [124
]. Additionally, this may result in fish attraction and aggregation when compared to surrounding soft-bottom areas [122
However, offshore structures may contribute to the propagation of NNS (including macroorganisms and microorganisms such as pathogens and parasites) in the marine environment, serving as “stepping stones” for the organisms [124
]. The introduction of NNS often impacts biodiversity, habitats or ecological processes, and it may pose both ecological and economical threats [12
Although requirements to biofouling control per se are non-existent worldwide, as a vector of NNS propagation, the biofouling aspect of maritime sectors has received attention especially in the last two decades and is now regarded in several international/European legislative frameworks (and in other national ones), for example:
2004: The United Nations International Maritime Organization (IMO; http://www.imo.org
) hosts the International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM) which provides standards and guidelines to prevent, minimize and furtherly eliminate the transfer of harmful organisms and pathogens in ballast waters and sediments.
2008: The EU Marine Strategy Framework Directive (MSFD, Directive 2008/56/EC; https://ec.europa.eu
) enters into force aiming at a more effective protection of the marine environment and biodiversity. The MSFD intends for the Members States to achieve “Good Environmental Status” with assessment of 11 Descriptors including the D2—Non-Indigenous Species
, through an adaptive management approach which must be kept up-to-date and reviewed every six years.
2011: The IMO Marine Environment Protection Committee (MEPC) adopts the IMO guidelines for the control and management of ships’ biofouling to minimize the transfer of invasive aquatic species (resolution MEPC.207(62)), which was further supplemented by the 2012 guidance for minimizing the transfer of invasive aquatic species as biofouling (hull fouling) for recreational craft (MEPC.1/Circ.792).
2015: The EU Regulation on invasive alien species (IAS Regulation 1143/2014; https://ec.europa.eu
) enters into force setting out rules to prevent, minimize and mitigate the adverse impacts caused by invasive species. The Regulation requires the Member States to study the introduction routes and spread of invasive species and to set up surveillance systems and action plans to ascertain the adequate preventive measures, among others.
Having all legislation pieces into account, it makes necessary to players in the MRE sector to develop biosecurity risk assessment/management plans aiming to predict and prevent the establishment and propagation of NNS as a condition of their projects. In this sense, the biofouling database presented in this paper could be especially useful since it provides beforehand a mapping of non-native species found across European waters. This awareness, in turn, may be helpful in the development of maintenance plans (mentioned in Section 2.4