Characterising the Second Wave of Fish and Invertebrate Colonisation

Home , Common dragonet, Dahlia anemone, Trachinotus ovatus

Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021 ICES Journal of Marine Science (2021), doi:10.1093/icesjms/fsaa245

Characterizing the second wave of ﬁsh and invertebrate colonization of an offshore petroleum platform

Victoria L. G. Todd1,2*, Irene Susini1, Laura D. Williamson 1,2, Ian B. Todd1, Dianne L. McLean3,4, and Peter I. Macreadie 5 1Ocean Science Consulting, Spott Road, Dunbar, East Lothian EH42 1RR, UK 2Environmental Research Institute, University of the Highlands & Islands, Thurso KW14 7EE, UK 3Indian Ocean Marine Research Centre, Australian Institute of Marine Science, Cnr. of Fairway and Service Road 4, Perth, WA 6009, Australia 4The UWA Oceans Institute, The University of Western Australia, 35 Stirling Hwy, Perth, WA 6009, Australia 5School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Burwood, VIC 3125, Australia *Corresponding author: tel: þ44 (0)1368 865722; e-mail: [email protected]. Todd, V. L. G., Susini, I., Williamson, L. D., Todd, I. B., McLean, D. L., and Macreadie, P. I. Characterizing the second wave of ﬁsh and invertebrate colonization of an offshore petroleum platform. – ICES Journal of Marine Science, doi:10.1093/icesjms/fsaa245. Received 3 June 2020; revised 19 November 2020; accepted 25 November 2020.

Offshore Oil and Gas (O&G) infrastructure affords structurally complex hard substrata in otherwise featurless areas of the seafloor. Opportunistically collected industrial ROV imagery was used to investigate the colonization of a petroleum platform in the North Sea 1– 2 years following installation. Compared to pre-construction communities and pioneering colonizers, we documented 48 additional taxa, including a rare sighting of a pompano (Trachinotus ovatus). The second wave of motile colonizers presented greater diversity than the pioneering community. Occurrence of species became more even over the 2 years following installation, with species occurring in more comparable abundances. No on-jacket sessile taxa were recorded during first-wave investigations; however, 17 sessile species were detected after 1 year (decreasing to 16 after 2). Motile species were found to favour structurally complex sections of the jacket (e.g. mudmat), while sessile organisms favoured exposed elements. Evidence of on-jacket reproduction was found for two commercially important invertebrate species - common whelk (Buccinum undatum) and European squid (Loligo vulgaris). Moreover, abundance of larvae-producing species experience an 8.5- fold increase over a 2-year period compared to baseline communities. These findings may have implications for decommissioning and resource-management strategies, suggesting that a case-by-case reviewing approach should be favoured over the most common “one size fits all”. Keywords: connectivity, decommissioning, infrastructure, jacket, marine, O&G platform, rigs-to-reefs, ROV

Introduction Todd et al., 2020), affording structurally complex hard substrata Offshore Oil and Gas (O&G) installations are becoming increas- for the settlement of sessile organisms in otherwise featureless ingly common globally, and 1350 O&G structures are operating areas of sea floor (Whomersley and Picken, 2003; Leit~ao et al., at present within the OSPAR maritime area (Arctic, Greater 2007; Joschko et al., 2008; Guerin, 2009; Vanagt et al., 2013; North Sea, Celtic Seas, Bay of Biscay, Wider Atlantic) alone Simons et al., 2016). The newly established hard-substrate (OSPAR Commission, 2017), most of which are accommodated community, in turn, creates novel feeding opportunities that can in the North Sea (Fowler et al., 2020). Subsea anthropogenic in- support diverse motile-benthic invertebrate and fish assemblages frastructure is known to act as artificial reefs (Guerin, 2009; (Vanagt et al., 2013; Todd et al., 2020). Kerckhof et al., 2010; Todd et al., 2018; Lacey and Hayes, 2020;

In addition to mere introduction of hard substrata, offshore Germany. The unmanned A18 satellite offshore-production plat- structures contribute to the creation of critical habitat and refugia form was installed on 4 October 2015 and lies ca. 300 km north of through their three-dimensional structure, therefore increasing Den Helder, Netherlands, in a water depth of ca. 47 m. Full site the ecological carrying capacity of specific areas (Wilson and description details can be found in Todd et al. (2020). Elliott, 2009). A habitat’s carrying capacity and hence the survival Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021 rate of its species are de facto functions of refuge availability for Videographic sampling and timings distinct life-history stages, with “habitat saturation” for a given General Visual Inspection (GVI) imagery from ROV surveys of stage possibly resulting in a bottleneck in production (Caddy and the A18 jacket was collected between 26–27 July 2016 and 8–15 Stamatopoulos, 1990; Caddy, 2008). When combined with in- May 2017 using a Tiger 828 and a Mohican A-Frame ROV. creased feeding opportunities, habitat creation enhances ecologi- Further details on ROV specifications, including speed, were not cal functioning and trophic efficiency alike (Bombace, 1989; available. Imagery was collected mostly (ca. 90%) during daylight Leit~ao et al., 2007; Wilson and Elliott, 2009). Highly productive hours, although a small percentage was collected during darkness systems, in turn, have potential to contribute substantially to bio- (shortly after sunset and shortly before sunrise). mass production (Nishimoto et al., 2019a), and records exist of juvenile reef fish recruits being more abundant at platforms than Video analysis at numerous natural sites (Claisse et al., 2014; Smith et al., 2016; Metadata, including depth, duration, file path, and name, were Nishimoto et al., 2019b). Reproductive strategies of species entered into an Excel spreadsheet, with one row representing recorded at subsea infrastructures (e.g. van der Molen et al., 2018; each video as per Todd et al. (2018, 2020). Nishimoto et al., 2019a, b) have led some to suggest that offshore The first stage of video analysis entailed screening for accep- constructions may also function as a network of interconnected tance or rejection using selection criteria based on a qualitative reef systems (i.e. “stepping stone” potential), facilitating species assessment of imagery quality, e.g. brightness, turbidity, and spe- range expansions and introduction of non-native taxa into novel cies visibility. Following initial screening, useable GVI imagery geographic areas through mechanisms of larval dispersal (Simons covered the entire water column of the platform (0 m to seabed at et al., 2016; van der Molen et al., 2018). ca. 46.8 m). Vertical and horizontal “sweeps” were performed by Despite the importance of the “production versus attraction” the ROV along each structure type, including caissons, conduc- debate in artificial-reef research, according to which structures ei- tors, and platform legs. A visual representation of investigated ther produce new biomass or simply attract existing organisms structural elements is presented in Figure 1. Additional details of (Pickering and Whitmarsh, 1997), there is still a profound need video screening processes are presented in Supplementary Section for improved scientific understanding of marine biota associated S1.1. with offshore infrastructure. This causes a number of issues, as hundreds of O&G installations (ca. 23 per year) are scheduled to be decommissioned in the next decade (OGUK, 2020). Sound sci- Taxonomic identification entific understanding improves accurate assessment of the poten- Taxonomic identification was performed on ROV video imagery tial net environmental benefit provided by anthropogenic according to Todd and Grove (2010) and Todd et al. (2018, structures. 2020) using identification guides and keys (e.g. Manuel, 1988; Todd et al. (2020) was the first study of its kind to report the Hayward et al., 1996; Hayward and Ryland, 1996; Miller and pioneer wave of fish and invertebrate colonization before and af- Loates, 1997; Maitland and Herdson, 2009) and various reputable ter placement of a new offshore production satellite platform in peer-edited online marine databases such as www.fishbase.org, the North Sea by analysing opportunistically collected industrial www.habitas.org.uk, www.sealifebase.ca, www.marlin.ac.uk, Remotely Operated Vehicle (ROV) data. The present study fol- www.marinespecies.org, http://species-identification.org, and lows on from Todd et al. (2020) by investigating and comparing www.algaebase.org. For the purpose of taxonomic identification, progressive species colonisation and production potential of the analysis of footage was preferred to the analysis of still images same (A18) platform 1 and 2 years after its initial installation. (discussed later) owing to the greater ease with which successful Diversity indices, relationships with structural complexity, and identification could be achieved. Taxa were identified through the reproductive strategy of observed species were investigated. comparison of ROV imagery with morphometric data/illustra- Analysis aimed to test the null hypotheses that (i) there would be tions (and for fish, meristics) and cross-referenced to known no significant variation in diversity indices of invertebrate and recorded habitat, distribution, ecology and depth preference for fish assemblages across a two-year period and (ii) no significant each identified taxon. Positioning within the trophic pyramid was differences in the relationship between community assemblages also identified using the above-mentioned resources. Specimens and distinct structural elements would be found. Lastly, recorded that could not be identified to species level were grouped into the taxa were identified to species level, when possible, and their re- next higher taxonomic level as per Lacey and Hayes (2020). productive strategies reviewed with regard to type (sexual versus asexual) to contribute to the ongoing “production versus Still-image collection and analysis attraction” debate put forward by Pickering and Whitmarsh Randomly timed still images, i.e. screen snapshots, were collected (1997). for each video as per McLean et al. (2019), resulting in an image every ca. 2 min. Random timing for the collection of stills was cal- Material and methods culated in Excel using the command Site description “¼RANDBETWEEN(bottom, top)”. ROV still imagery was ana- A18 Block is located in the Netherlands sector of the Southern lysed visually by the same analyst to avoid observer bias. The na- Gas Basin in the North Sea and shares a grid pattern with ture of GVI footage ensured that each still presented comparable The second wave of fish and invertebrate colonization 3 Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 1. Investigated platform structural elements with associated quantity: legs or VM (4), HM (25), horizontal diagonal members (HDM, 13), vertical diagonal members (VDM, 20), and conductors (CON, 3). Weight: 950 tonnes (topside), 1250 tonnes (jacket). Source: adapted from HSM Offshore (2014). sections of structure surface. Evaluation of still images was per- Reproductive-strategy analysis formed using PhotoQuad v1.4 as per Trygonis and Sini (2012). Specimens identified reliably to species level were grouped into One hundred points were used in a stratified random grid (10 the following reproductive guilds: basal laceration, broadcast 10) to gain even coverage of the entire image as per Gormley spawner, juvenile–adult producer, larvae producer, passive et al. (2018). An example of this is presented in Figure 2. Each drifter, polyp producer, substratum-egg layer, and zoospore pro- point was assigned to a taxon or structure type (e.g. platform and ducer. Identification of reproductive guilds was performed using ROV tether). Identification of species was assisted by the species taxon-specific peer-reviewed papers and the same reputable peer- identification library developed during video analysis. Frequency edited online marine databases used for taxonomic identification of occurrence was calculated based on the number of points cor- (see “Taxonomic identification” section). Egg- and larvae- responding to each taxon/structure type in each still image (e.g. producing species regarded largely as broadcast spawners were out of 100 points in total, 50 could have corresponded to species assigned distinct guilds to account for differences in propagule A, 25 to species B, 10 to species C, and 15 to water). Water was nature (e.g. fish as broadcast spawner and Asteroidea as larvae recorded in PhotoQuad, although excluded from statistical analysis. Only species data were converted into frequency of occur- producers). Species that crossed categories, such as some ane- rence, with a new total (i.e. <100) created accordingly. Moreover, mones (e.g. sexual versus asexual, Bocharova and Kozevich, the young nature of the A18 platform at the time of investigation 2011), were classified as asexual reproducers when a preferred re- ensured that only a negligible proportion of overgrowing layers of productive strategy could not be identified reliably. This was epifauna (which could bias frequency of occurrence estimation) done to obviate production-potential overestimation. Despite was encountered during analysis. This frequency-of-occurrence- reproducing both sexually and asexually, Asteroidea are regarded estimation method is suitable for sessile species; however, when a more commonly as larvae producers (e.g. Lein, 2016) and were still captures a motile species, such as a fish, an artefact of the therefore classified as such supported by evidence that Asteroidea technique is that it also designates the fish as “frequency of tend to reproduce sexually in the Atlantic (Garcia-Cisneros et al., occurrence”. For those motile species in the water column, this 2015). consequently increases or decreases “frequency of occurrence” accordingly, depending on the closeness of the fish to the ROV lens. Data analysis To minimize bias, it was ensured that only one point was assigned For consistency, the majority of data analysis was performed as to motile species close to the ROV lens. Similarly, in the instance per Todd et al. (2018, 2020), where species richness (S), abun- of multiple points being assigned to an isolated mobile organism dance (N), and Shannon diversity (H0) were assessed at different (e.g. fish, mobile crustacean, starfish), the random points were water depths. In addition, evenness (E) and Simpson’s domi- generated anew until a single point was assigned to the organism nance (D) indices—both constrained values between 0 and 1— in question. were estimated at different depths. During analysis, the “Simpson dominance method” returned a “dominance index”; the higher the value, the lower the diversity (Magurran, 2013). This is 4 V. L. G. Todd et al. Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 2. Example of ROV imagery showing stratiﬁcation grid (red lines) and random-stratiﬁed points (yellow stars) that were used to analyse frequency of occurrence for sessile species. Image cropped slightly to remove commercially sensitive information.

and was not considered further. Data were grouped by depth band as per Figure 4a for sessile species (5-m interval) and Figure 4b for motile species, the latter of which were grouped ini- tially in the ca. 6-m interval and then ca. 15-m interval thereafter. Differential use of depth bands for the two species categories was necessary due to the nature of the GVI imagery survey method, in that data were collected in each section of water column separat- ing consecutive horizontal members (HMs) (i.e. elevation 0–6, 6– 20, 20–34.5, 34.5–44.5, and 44.5þ m) by performing up-and- down sweeping movements along all structural elements in each section; however, use of 5-m depth bands allowed finer resolution of vertical trends and was therefore used for sessile species. The pre/post-installation surveys presented in Todd et al. (2020) were performed only on depth band 40–44.99 m, which means that only this depth could be compared across 2015, 2016, and 2017 data sets. Statistical analysis was performed in R version 3.6.2 (R Core Team, 2019) using packages tabula (Frerebeau, 2019) and vegan (Oksanen et al., 2019). Frequency of occurrence and count data Figure 3. Visual representation of the inverse relationship between were assessed by applying a-diversity analysis, as per Todd et al. heterogeneity (or diversity in terms of H0 and E) and dominance (in (2018, 2020). Statistical significance was set at a ¼ 0.05. terms of D). An ANalysis Of SIMilarity (ANOSIM) test was performed on data from 2016 and 2017 to determine fouling community simi- demonstrated in Figure 3 to facilitate the interpretation of results. larities across depth bands, with a separate SIMilarity of Further explanation of indices is provided in Supplementary PERcentage (SIMPER) analysis to define which fouling category Section S1.2. expressed the largest contribution to dissimilarity between depth H0 and D were converted to Effective Number of Species bands. Both ANOSIM and SIMPER analyses were conducted us- (ENS) as per Jost (2006). S, H0, E, and D were calculated sepa- ing 5-m interval depth bands as per the analysis of sessile- rately for motile and sessile species. For the former, a number of community diversity. Non-Metric Multi-Dimensional Scaling observations were used; for the latter, frequency of occurrence (NMDS) ordination was applied to a corresponding Bray–Curtis was estimated. N was scaled to “1” for each image still analysed similarity matrix to identify groupings of similar species. A The second wave of fish and invertebrate colonization 5 Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 4. Investigated depth bands for (a) sessile and (b) motile species. Source: adapted from HSM Offshore (2014).

Pearson’s chi-square test was performed successively to investi- Table 1. Breakdown of still numbers per depth band and year. gate existence of an association between species occurrence and jacket structural complexity in a method adapted from Consoli Depth band (m) Stills (2016) Stills (2017) Total stills et al. (2018). From least to most structurally complex: not touch- 0–4.99 17 4 21 ing member, HM, VM ¼ vertical member, DM ¼ diagonal mem- 5–9.99 78 43 121 10–14.99 18 6 24 ber, J2M ¼ junction of two members, J3M ¼ junction of three 15–19.99 32 18 50 members, J4M ¼ junction of four members, and M ¼ mudmat. 20–24.99 48 34 82 HM, VM, and DM were regarded as being of comparable com- 25–29.99 22 4 26 plexity, as they were all individual members, differing solely in 30–34.99 44 25 69 spatial orientation. Only motile (some invertebrate and fish) and 35–39.99 77 31 108 sessile invertebrate species were included in the analysis. Marine 40–44.99 97 53 150 algae, Serpulidae, and holoplanktonic organisms (e.g. jellyfish 45þ 187 96 283 and ctenophores) were excluded due to their extensive, unspecific Total 620 314 934 distribution observed during imagery and still analysis. Lastly, de- scriptive statistics of proportions was conducted on reproductive- strategy data to assess the amount of species by reproductive was that of secondary consumers (III), which included a mixture strategy. of fish, echinoderms, cnidarians, gastropods, and ctenophores. The remaining trophic levels were, nonetheless, well represented. Results Figure 5 presents a comparison of phyla occurrence over the 3 A total of 201 videos (hTot ¼ 25:03) and 934 stills (1,231 1,001 years, revealing a clear increase in taxa presence with increasing pixels) were viewed and used in analyses. Screening for the accep- jacket age, especially fish, followed by arthropods, and molluscs. The tance/rejection of imagery was conducted, and all data were newly installed and “clean” 2015 A18 jacket lacked taxonomic vari- deemed usable for analysis. Table 1 presents a breakdown of ana- ety, with some motile species, e.g. ctenophores, and sessile categories lysed stills per depth band and year. absent compared to 2016 and 2017, when all categories were represented. In the later years, juvenile gadoids were also recorded, as Taxonomic identification they were easy to distinguish compared to other juvenile fish, which Table 2 presents a list of species recorded on/around the jacket were difficult to identify and thus not considered. A sample of ROV over the investigated years, categorised into four trophic levels images are presented in Figure 6.Ofnoteisthesightingoftheva- and reproductive guilds. In total, eleven phyla comprising 56 spe- grant pompano, Trachinotus ovatus (Figure 6s). cies and one unidentified jellyfish were observed. Compared to 2015 (Todd et al., 2020), 48 additional taxa were documented, the majority of which were chordates (predominantly fish); however, examination of the same section of the jacket that was inves- Diversity indices tigated in 2015 only yielded an additional 25 species. No sessile Detailed explanations on interpretation of indices are provided in taxa were recorded on the new jacket during first-wave investiga- Jost (2006) and Magurran (2013), and a recap is presented in tions (2015); however, 17 sessile species were detected after 1 year, Supplementary Section S2, together with tables and trend charts decreasing to 16 after 2. The most highly populated trophic level for both motile and sessile species. 6 V. L. G. Todd et al.

Table 2. Taxa recorded at A18 jacket during 2016–2017 with associated trophic level and species richness (S): I (primary producers, S ¼ 3), II (primary consumers, S ¼ 12), III (secondary consumers, S ¼ 29), and IV (tertiary consumers, S ¼ 10). Trophic Reproductive Motile/

Phylum level guild sessile Common name Lowest taxonomic ID Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021 Annelida I LP Sessile Tube worm Serpulidae Arthropoda II LP Sessile Barnacle Chirona hameri III LP Motile Edible crab Cancer pagurus III LP Motile Hermit crab Pagurus bernhardus II LP Motile Krill Euphausiacea III LP Motile Masked crab Corystes cassivelaunus III LP Motile Norway king crab Lithodes maja III LP Motile Rugose squat lobster Munida rugosa II JAP Motile Skeleton shrimp Caprellidae Bryozoa II LP Sessile Turf Bryozoa Bryozoa Chordata IV BS Motile Atlantic cod Gadus morhua IV BS Motile Bib Trisopterus luscus III BS Motile Blenny Blenniidae III BS Motile Common dab Limanda limanda III BS Motile Common dragonet Callionymus lyra III BS Motile Common sole Solea solea III BS Motile European flounder Platichtys flesus III BS Motile Five-bearded rockling Ciliata mustela III BS Motile Flatfish Pleuronectiformes IV BS Motile Haddock Melanogrammus aeglefinus IV BS Motile Horse mackerel Trachurus trachurus IV BS Motile Pompano Trachinotus ovatus IV BS Motile Pollock Pollachius pollachius IV BS Motile Poor cod Trisopterus minutus III BS Motile Red mullet Mullus barbatus III BS Motile Right-eyed flounder Pleuronectidae II LP Sessile Sea squirt Ciona intestinalis III BS Motile Wrasse Labridae IV BS Motile Whiting Merlangius merlangus Cnidaria III PP Motile Blue jellyfish Cyanea lamarckii III LP Sessile Cup coral Caryophyllia smithii. III LP Sessile Dahlia anemone Urticina felina III LP Sessile Dead man’s fingers Alcyonium digitatum III LP Sessile Deeplet anemone Bolocera tuediae III BL Sessile Elegant anemone Sagartia elegans III PP Motile Lion’s mane jellyfish Cyanea capillata II PP Sessile Oaten-pipes hydroid Tubularia indivisa III BL Sessile Plumose anemone Metridium sp. III PP Motile Unidentified jellyfish – Ctenophora III PD Motile Common northern comb Bolinopsis infundibulum jelly III PD Motile Pink slipper comb jelly Beroe cucumis III PD Motile Sea gooseberry Pleurobrachia pileus Echinodermata III LP Motile Bloody Henry sea star Henricia oculata III LP Motile Common sea star Asterias rubens II LP Motile Sea urchin Echinus sp. III LP Motile Sand sea star Astropecten irregularis Mollusca IV SEL Motile Common cuttlefish Sepia officinalis IV SEL Motile Common squid Loligo vulgaris III SEL Motile Common whelk Buccinum undatum III SEL Motile Dog whelk Nucella lapillus II LP Sessile European flat oyster Ostrea edulis II LP Sessile Great scallop Pecten maximus II LP Sessile Mussel Mytilus sp. Ochrophyta I ZP Sessile Brown algae Ectocarpus sp. Porifera II LP Sessile Demosponge Amphilectus fucorum II LP Sessile Sponge (possibly common) Suberitidae Rhodophyta I ZP Sessile Red algae Corallinaceae Reproductive guilds are also reported: BL ¼ basal laceration, BS ¼ broadcast spawner, JAP ¼ juvenile-adult producer, LP ¼ larvae producer, PD ¼ passive drifter, PP ¼ polyp producer, SEL ¼ substratum egg layer, and ZP ¼ zoospore producer. Grey cells indicate species recorded in 2015 by Todd et al. (2020). Species are in alphabetical, not taxonomical order. The second wave of fish and invertebrate colonization 7 Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 5. Comparison of phyla occurrence in 2015 (pre- and immediately post-installation) and 2016–2017.

Figure 6. Sample of species recorded on/around the A18 jacket during 2016–2017: (a) Alcyonium digitatum, (b) Asterias rubens, (c) Astropecten irregularis, (d) Beroe cucumis, (e) Bolinopsis infundibulum, (f) Buccinum undatum with egg masses, (g) Cancer pagurus, (h) Caryophyllia smithii, (i) Corystes cassivelaunus, (j) Cyanea capillata, (k) Gadus morhua, (l) Loligo vulgaris egg mass, (m) Melanogrammus aegleﬁnus, (n) Merlangius merlangus, (o) Metridium sp., (p) Mytilus sp., (q) Mullus barbatus, (r) Pollachius pollachius, (s) Trachinotus ovatus, and (t) Trisopterus luscus. Species are presented in alphabetical order.

Motile species jacket. When considering separate signiﬁcance of such changes Diversity indices (S, H0, E, D) at each depth band from 2016 and in relation to one another, a community-level increase in overall 2017 were compared to those in the 2015 Todd et al. (2020) base- diversity is evidenced. While the total number of motile species line study. decreased from 2016 to 2017 (Figure 7a), a diversity of the Figure 7 illustrates temporal changes in investigated diversity resulting community remained relatively stable over time indices for the motile species community on/around the A18 (Figure 7b). Moreover, despite a decrease from 2015 levels (pre and post), distribution of recorded species became more even 8 V. L. G. Todd et al. Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 7. Change in investigated diversity indices for motile species (n ¼ 32) across depth bands in 2015 (pre- and immediately post- installation), 2016, and 2017. (a) Species richness (total number of species in the community), (b) Shannon diversity (index), (c) evenness (frequency distribution of species), and (d) Simpson’s dominance index (proxy of dominance). Vertical line indicates arbitrary threshold (0.5) between low/high values. Arrow indicates nature of observed trend (increasing/decreasing): black—both 2016–2017, red—2016, and blue— 2017. between 2016 and 2017 (E entirely >0.5 in 2017, Figure 7c), Table 3. Means of diversity indices with associated 95% confidence and levels of dominance decreased from baseline estimates interval (CI). (D < 0.5), indicating an increase in community-level heteroge- 95% CI neity (low dominance ¼ high heterogeneity, Figure 7d). In 2016–2017, diversity indices exhibited relatively consistent 2015 2015 trends across depth bands: S and H0 increased generally with in- Index (pre) (post) 2016 2017 creasing water depth, E remained relatively constant, and D de- Species richness (S) 7 11 13.8 6 3.48 11 6 5.2 creased, especially in 2017. No statistical analysis, however, Shannon diversity (H0) 1.65 1.48 1.38 6 0.36 1.47 6 0.38 could be conducted on diversity indices across depth bands, as Evenness (E) 0.85 0.62 0.53 6 0.13 0.66 6 0.09 only one estimate was available per sample (depth band). Simpson’s dominance (D) 0.75 0.67 0.36 6 0.15 0.32 6 0.13 Supplementary Table S5 presents H0-andD-derived ENS (here- 2015 (pre and post) had n ¼ 1 and CIs all equalled zero. after ENSH0 and ENSD, respectively), and Supplementary Figure S2 illustrates ENS trends over time and across depth bands. Lowsamplesize(n ¼ 5) translated to low statistical power. The indicating low community-level heterogeneity (high dominance mean indices values (with 95% confidence interval) are, there- ¼ low heterogeneity, Figure 8d). Across depth bands, S exhibited fore, presented (Table 3). contrasting patterns, remaining relatively stable in 2016 and increasing with water depth in 2017; H0 and D remained unaltered; Sessile species E exhibited a fluctuating pattern in 2016; and it tended to de- Figure 8 illustrates temporal changes in investigated diversity increase with increasing depth in 2017. No statistical analysis, how- dices of the sessile-species community on/around the A18 jacket. ever, could be conducted on diversity indices across depth bands, Again, when considering separate significance of such changes in as only one estimate was available per sample (depth band). relation to one another, a generally low community-level diversity Supplementary Table S7 presents ENSH0 and ENSD, and is evidenced; however, as no sessile taxa were recorded in 2015, Supplementary Figure S3 illustrates ENS trends over time and across depth bands. S and E exhibited statistically significant dif- low estimates represent, nonetheless, an increase from baseline ferences between 2016 and 2017 (two sample t-test, S: t ¼ conditions. While total number of sessile species increased from 18 2.25, p ¼ 0.037; E: t ¼ 2.686, p ¼ 0.015); however, H0 and D 2016 to 2017 (Figure 8a), diversity of the resulting community 18 failed to exhibit such differences (two sample t-test, H0: t ¼ remained unaltered over time (Figure 8b). Moreover, distribution 18 0.22, p ¼ 0.828, D: t ¼0.244, p ¼ 0.81). of recorded species became less even between 2016 and 2017 (E 18 almost entirely <0.5 in 2017, Figure 8c), and levels of dominance (D) remained elevated (and unaltered) over time (D > 0.5), The second wave of fish and invertebrate colonization 9 Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 8. Change in investigated diversity indices for sessile species (n ¼ 12) across depth bands in 2015 (pre- and immediately post- installation), 2016, and 2017. (a) species richness (total number of species in the community), (b) Shannon diversity (index), (c) evenness (frequency distribution of species), and (d) Simpson’s dominance index (proxy of dominance). Vertical line indicates threshold (0.5) between low/high values. Arrows indicate nature of observed trend (increasing/decreasing): black—both 2016–2017, red—2016, and blue—2017.

Figure 9. NMDS of species/groups detected in still images and depth bands. Red-circled numbers indicate depth bands, and black text indicates species/groups. Ellipses identify groupings. Red arrow points to exact location of grouped species.

Species assemblages and “obligate epi-benthic” groups presented the highest num- Difference in colonization–assemblage similarity between depth ber of species unique to the group, i.e. found in no other depth bands was found to be statistically significant (ANOSIM, band (nine and six, respectively). Conversely, groupings A and R ¼ 0.2355, p ¼ 0.001); however, depth bands exerted a relatively B presented a single group-specific taxon, i.e. unidentified jelly- small effect on species assemblages, as demonstrated by the R value fish and Dahlia anemone (Urticina felina), respectively; how- (i.e. 0.2355) being closer to 0 than 1 (R constrained between 0 and ever, both species accounted for a single observation. Despite 1). Figure 9 presents the four distinct groupings of species and elevated number of species unique to “deep-water” group, depth bands that were identified through MDS, of which “deep- SIMPER analysis identified marine algae and Serpulidae alone water” group (depths 25–45þ m) accounted for the highest num- as responsible for the most dissimilarity between depth bands. ber and greatest variety of species (both motile and sessile). Although to a lesser extent, common starfish (Asterias rubens) A complete list of taxa detected in each depth group is pro- was also found to contribute to differences between depth vided in Supplementary Section S3, revealing that “deep-water” bands. SIMPER dissimilarity indices (%) for recorded species 10 V. L. G. Todd et al. Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 10. Scaled frequency of occurrence of species groups in each depth band in 2016–2017. Percentage of uncolonized structure is not included. in each investigated depth band are presented in Reproductive-strategy composition Supplementary Section S3. Figure 12 presents temporal changes experienced by on-jacket reproductive-strategy composition. Spatial distribution Immediately post-installation, communities (i.e. 2015) were Figure 10 presents scaled frequency of occurrence of recorded dominated by species reproducing via broadcast spawning (see taxonomic groups for each depth band. Fish (primarily Gadidae) Todd et al., 2020). These included common dab (Limanda were recorded in both shallow (10–20 m) and deep areas, al- limanda), common dragonet (Callionymus lyra), and whiting though they were most prevalent at depths of 40þ m. Bib (Merlangus merlangus). Larval production was the second most (Trisopterus luscus) was the most common and abundant of the common strategy (two species), followed by polyp production gadoid species and occurred mostly at 40þ m. Marine algae and substratum-dependent egg laying (one species each). (Corallinaceae and Ectocarpus sp.) and Annelida (Serpulidae) rep- Number of larvae-producing taxa increased from 2 to 17 in 2015 resented the most common groups overall. Despite their co- and 2016, respectively, with larval production becoming the dom- occurrence, the two groups were recorded in a contrasting pat- inant reproductive strategy. Composition remained consistent in tern, with marine algae dominating the first half of the water col- 2017, with larval production (14 species) and broadcast spawning umn and Serpulidae most abundant when algae abundance was (eight species) most common; however, passive drifters (e.g. lowest. Bryozoa and Porifera accounted for a negligible percent- Ctenophora) increased from 1 to 4 representatives in 2016 and age of total occurrences and are therefore not clearly visible in 2017, respectively, becoming the third most common reproduc- Figure 10; however, they are present at depths of 45þ m. tive guild. A statistically significant correlation was found between species occurrence and jacket structural complexity (Pearson’s chi-square 2 Discussion test: X 105 ¼ 488.61, p < 0.001). This is demonstrated graphically in Figure 11, which reveals that the M, i.e. high-complexity base Taxonomic identification of jacket, was occupied by the greatest number of species. These Over 25 h of industrially collected ROV imagery were analysed, comprised predominantly non-benthic motile taxa, especially resulting in the detection of 56 species on the A18 jacket, an in- fish. Conversely, sessile organisms appeared to favour, generally, crease of 48 species over the pre- and immediately post- HM and VM, as well as DM and J2M to a lesser extent. Species installation findings in Todd et al. (2020); however, three species that tended to occur at a distance from the jacket (e.g. water col- were not re-sighted in later years: swimming crab (Liocarcinus umn/seabed) were assumed to have no affiliation with particular holsatus), grey gurnard (Eutrigla gurnardus), and razor shells structural members for the purpose of the present analysis. Their (Ensis sp.). Pre- and immediately post-installation communities distance from members, however, may be an artefact of imagery- were dominated by fish taxa (Chordata), with hard-substrata data collection and it should not be interpreted as a lack of affilia- dwelling invertebrates virtually absent due to infrastructure hav- tion with the jacket. A breakdown of stills analysed and sample ing been in situ for only four days. Six new phyla (Annelida, size is presented in Table 4 for each complexity category. Bryozoa, Ctenophora, Ochrophyta, Porifera, and Rhodophyta) were documented on the jacket in 2016, i.e. 1 year following in- Reproductive potential stallation. Such phyla persisted in 2017. Moreover, fish species Evidence of on-jacket reproduction in the form of egg masses was exhibited a three- to fivefold increase between 2015 and subse- recorded for two invertebrate species, i.e. common whelk quent years, suggesting that colonization of sessile invertebrates (Buccinum undatum) and European squid (Loligo vulgaris), dur- supported a greater number and diversity of benthic/pelagic pred- ing both 2016 and 2017. ators (Moreau et al., 2008; Vanagt et al., 2013). The second wave of fish and invertebrate colonization 11 Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 11. Species number (n) as a function of jacket structural complexity: n ¼ number of observations.

Table 4. Number of stills analysed for each complexity category and contributes to creation of refugia through its three-dimensional associated sample size. structure (Pontarp and Wiens, 2017), which, in turn, can accom- modate a greater number of species that would otherwise be ab- Complexity category Sample size sent from sand-only habitats; however, it is also possible that Away from member 48 presence of new habitat simply intercepted larvae and fish that Horizontal member 59 would have settled elsewhere had the jacket been absent VM 60 DM 30 (Nishimoto et al., 2019a). The second wave of jacket colonisation J2M 51 documented in this study appears to have a relatively even distri- J3M 19 bution of new colonisers (S) amongst four trophic levels. High J4M 2 species richness across multiple trophic groups (i.e. multitrophic M79richness) has been shown to exert stronger positive effects on eco- Total 348 system functioning than elevated species richness in any individual trophic group (Soliveres et al., 2016); therefore, change in number and trophic structure of species recorded around the A18 The pompano, T. ovatus (family Carangidae), was an unusual jacket may be interpreted as an initial step towards high ecosys- observation. As opposed to the Atlantic horse mackerel tem functionality. (Trachurus trachurus), regarded as the only common member of A better understanding of underlying processes that have led the Carangidae family to occur in northern European seas, T. to the community structure that exists on the jacket requires on- ovatus occurs as a rare vagrant in waters north of the southern going surveys; however, this required level of sampling, while Mediterranean Sea (Lloret et al., 2015; Villegas-Hernańdez et al., ideal for improving our ecological understanding, is unlikely to 2016). To the best of our knowledge, no peer-reviewed evidence occur where it does not align with engineering-inspection time- of the species occurring in the North Sea exists to date, and repu- lines. Industry support of additional scientific research that aims table, peer-edited marine databases appear to have contradicting to better understand the influence their structures have in marine information on the species’ distribution (e.g. FishBase maintains ecosystems is required (McLean et al., 2020). T. ovatus does not occur in the North Sea, while IUCN argues the opposite); therefore, this study affords, possibly, the first pub- Motile species lished record of T. ovatus in the North Sea region. The motile-benthic community that characterized the A18 jacket in 2016–2017 exhibited apparent increases in diversity over time Diversity indices and across depth bands, although these were arguably negligible. Diversity indices were calculated to enable comparison between The community also exhibited greater heterogeneity than pre- 2015 and 2016–2017 data; however, as only a fraction of data and immediately post-installation assemblages. Such an increase were analysed, discussed trends are not to be interpreted as appli- was accompanied, however, by lower cross-species evenness in cable to the entire epifauna and motile communities but rather as abundance, demonstrated by the discrepancy between ENSH0 and an indication of colonisation trends over time. ENSD, respectively, and the actual number of total species A substantial increase in S estimates was recorded for both mo- recorded (S). This is likely ascribable to the community having tile and sessile species over the two years following jacket installa- yet to reach maximum carrying capacity. Increased numbers of tion. Possible explanations for this increase include enhanced species translate, plausibly, into increased community diversity; carrying capacity, as introduction of offshore infrastructure however, as colonization processes require time (Taylor and 12 V. L. G. Todd et al. Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021

Figure 12. Change in reproductive-strategy composition of species around A18 jacket with time.

Wilson, 2003), these were likely on-going at the time of investiga- composition across depth bands, possibly due to the limited tion and self-sustaining, viable populations were yet to be estab- number of within-taxon observations included in the study. lished for new colonizers. Furthermore, shallowness of the area may have encouraged occurrence of taxa with similar depth preference. Sessile species Noteworthy is the recorded association of 0-group (i.e. first Compared to motile species diversity, the sessile community year of life) gadoid fish and Scyphozoan lion’s mane jellyfish exhibited lower community-level heterogeneity and uneven oc- (Cyanea capillata). 0-group gadoids were recorded sheltering be- currence of species. Marine algae (Ectocarpus sp. and neath the jellyfish umbrella, finding refuge among its tentacles. 0- Corallinaceae), together with tube worms (Serpulidae), domi- group gadoids inhabiting the North Sea, M. merlangus in particular, may benefit from greater survival rate to the 1-group stage as nated sessile assemblages, which likely reduced overall commu- a direct result of the commensal relationship described above nity diversity. This is supported by low ENS 0 and ENS , which H D (Hay et al., 1990). This is of importance when speculating about never exceeded two. Moreover, elevated dominance estimates the role offshore platforms play in marine ecosystems. Presence (D > 0.5) also suggest low diversity. Dominance and even- mean of C. capillata may be supported by, inter alia, increased prey ness are often regarded as complementary diversity measures availability (Decker et al., 2018) and enhanced population con- (Magurran, 2013), as a community presenting a sub-set of species nectivity resulting from introduction of offshore platforms with a higher occurrence-frequency rate than others is necessarily (Vodopivec et al., 2017). In turn, increased abundance of jellyfish characterized by unequal distribution of species. Nonetheless, low provides shelter and foraging opportunities to commercially im- evenness, along with high numbers of species, has been associated portant 0-group gadoids which, as opposed to demersal adults, with enhanced ecosystem multifunctionality (Maestre et al., 2012; inhabit the upper water layers (40 m) for a period of months Lefcheck et al., 2015). Therefore, it is plausible to assume that the (Bjørke and Saetre, 1994). A18 ecosystem will experience a rise in functionality as a result of progressive colonization and subsequent increase in sessile species Spatial distribution occurrence. A statistically significant association was found between species occurrence and jacket structural complexity. M, the structure pre- Species assemblages venting offshore infrastructure from sinking into unconsolidated In accordance with previous research on depth zonation on off- soil (Yarrarapu, 2015), presented the highest frequency of species shore platforms (Whomersley and Picken, 2003), and despite the occurrence overall, supporting deep-water communities through jacket being located in shallow waters (<50 m), four distinct its multidirectional structure. Commercially important species assemblages of species and depth were identified: (i) shallow- (see EEA, 2017), including crustaceans (edible crab, Cancer pagu- water, (ii) mid-column, (iii) deep-water, and (iv) epi-benthic spe- rus), fish (Atlantic cod—Gadus morhua, haddock— cies. The latter did not associate significantly with any depth Melanogrammus aeglefinus, M. merlangus, red mullet—Mullus band, as such species only occurred at the lowest limit of the last barbatus, European flounder—Platichthys flesus, common sole— depth band (i.e. seabed). The identification of species assemblages Solea solea), and molluscs (B. undatum and L. vulgaris) exhibited did not exhibit statistically significant dissimilarities in species different location preferences; however, they all tended to occur The second wave of fish and invertebrate colonization 13 at greater depths in the vicinity of the M. This is likely explained estimated increase of ca. 88 and 86%, respectively, compared to by demersal distribution of the abovementioned species. 2015. Abundance of broadcast spawners also increased, exhibiting Non-benthic motile taxa and sessile organisms appeared to ex- substantial growth in 2016–2017 (ca. 79 and 62%, respectively). press habitat-preference differences. The former (in particular Such increases in larval production are consistent with progres- Downloaded from https://academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsaa245/6145865 by University of Aberdeen user on 22 February 2021 fish, including commercially important gadoids) appeared to fa- sive establishment of on-jacket epifauna (sessile) communities vour complexity and shelter afforded by the M. These results are documented by the present study in the years following consistent with previous research, which found that increasing installation. habitat complexity resulted in an increase in fish abundance and Prevalence of propagule production around the A18 jacket car- species richness (e.g. Love et al., 2019). In fact, more complex ries important implications for biomass production at ecosystem structures have been shown to afford a number of benefits, in- level (Nishimoto et al., 2019a). Pelagic propagules can disperse cluding shelter from water currents and predation (Kovalenko considerable distances from the point of release (van der Molen et al., 2012), increased foraging opportunities (Fowler et al., et al., 2007), and reproductive strategies recorded at subsea infra- 2018), and spawning substrate (McLean et al., 2017; Todd et al., structures thus far have led some to suggest some offshore struc- 2018). tures may function as a network of interconnected reef systems Conversely, sessile organisms were found to associate predomi- (i.e. “stepping-stones”), facilitating species range expansions nantly with horizontal and VMs, as well as with DMs and junc- through mechanisms of larval dispersal (van der Molen et al., tions of two elements, albeit to a lesser extent. Such structures are 2018). significantly more exposed than M or member junctions and may have experienced greater settlement success by being intercepted Conclusions more readily than the rest of the jacket (Nishimoto et al., 2019a). This likely results in reduced swimming time, lowering energy Forty-eight additional taxa were recorded on the A18 jacket 1– expenditures associated with habitat search and contributes po- 2 years after installation compared to pre- and immediately tentially to higher fitness (Pinochet et al., 2020). Moreover, exposed surfaces likely afford access to greater flows of food post-installation; particles, favouring establishment of filter-feeding communities A carangid species (T. ovatus) was recorded, despite occurring (Thorpe, 2012). Although different sessile species exhibited di- only as a rare vagrant in the North Sea; verse preferences, they tended to avoid junctions between multi- The second wave of motile species colonization suggested ple (>2) members. greater diversity compared to baseline communities; however, no statistically significant differences in diversity indices were Reproductive potential found between 2016 and 2017; Statically significant differences in species richness and even- Evidence of on-jacket reproduction was found for B. undatum ness estimates were found between 2016 and 2017 for sessile and L. vulgaris, both commercially important species in the species; United Kingdom and wider International Council for the Non-benthic motile taxa favoured complex, sheltered habitats Exploration of the Sea (ICES) area (Shrives et al., 2015; (M), and sessile organisms favoured more exposed surfaces Emmerson et al., 2018). Buccinum undatum is an obligate substratum egg layer, with females depositing eggs on hard substrata (horizontal/vertical); along the seabed (Kideys et al., 1993). The species lacks a dis- Depth bands exerted a statistically significant, albeit weak, ef- persed, pelagic stage and tagging studies have revealed adults to fect on fouling assemblages; and be relatively sedentary (Hancock, 1963, cited in Shrives et al., Evidence of on-jacket reproduction (egg capsules) was found 2015). This, when considered together with presence of numerous for two commercially important invertebrate species: B. unda- egg masses on the jacket, may have important ramifications for tum and L. vulgaris. local gastropod fisheries. Presence of a 500-m exclusion zone around offshore platforms (Kashubsky and Morrison, 2013), to- Supplementary data gether with currents and jacket architecture, prevents use of sev- Supplementary material is available at the ICESJMS online ver- eral types of fishing gear and may thus “transform” the site into a sion of the manuscript. de facto Marine Protected Area (Schroeder and Love, 2002). This would encourage B. undatum population development, poten- Acknowledgements tially benefitting fisheries in the future, should platform-fisheries General Visual Inspection (GVI) imagery from ROV surveys of compatibility be achieved (e.g. Fayram and De Risi, 2007). A sim- the A18 platform was collected by Bluestream Offshore B.V. and ilar case may be argued for L. vulgaris, its fast-growing nature N-Sea and provided by Petrogas E&P Netherlands B.V. (Moreno et al., 2012) facilitating substantial biomass contribution to the broader North Sea ecosystem in the absence of anthropo- Data availability statement genic pressure (e.g. fishing). The data underlying this article were provided by Petrogas by permission. Data will be shared on request to the corresponding Reproductive-strategy composition author with permission of Petrogas. As a result of changes in species occurrence, a marked change in reproductive-strategy composition was recorded. Pioneering References communities were dominated by broadcast spawners, reflecting Bjørke, H., and Saetre, R. 1994. Transport of larvae and juvenile fish the prevalence of fish taxa; however, a sharp increase in larvae- into central and northern Norwegian waters. Fisheries producing species was observed in 2016 and 2017, with an Oceanography, 3: 106–119. 14 V. L. G. Todd et al.

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Handling editor: Silvana Birchenough