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Size/Age Models for Monitoring of the Pink Sea Fan Eunicella Verrucosa (Cnidaria: Alcyonacea) and a Case Study Application

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Size/Age Models for Monitoring of the Pink Sea Fan Eunicella Verrucosa (Cnidaria: Alcyonacea) and a Case Study Application Journal of Marine Science and Engineering Article Size/Age Models for Monitoring of the Pink Sea Fan Eunicella verrucosa (Cnidaria: Alcyonacea) and a Case Study Application Giovanni Chimienti 1,2,* , Attilio Di Nisio 3 and Anna M.L. Lanzolla 3 1 Department of Biology, University of Bari Aldo Moro, Via Orabona 4, 70125 Bari, Italy 2 CoNISMa, Piazzale Flaminio 9, 00196 Roma, Italy 3 Department of Electrical & Information Engineering (DEI), Polytechnic University of Bari, 70125 Bari, Italy; [email protected] (A.D.N.); [email protected] (A.M.L.L.) * Correspondence: [email protected]; Tel.: +39-080-544-3344 Received: 26 October 2020; Accepted: 19 November 2020; Published: 22 November 2020 Abstract: The pink sea fan Eunicella verrucosa is a habitat-forming octocoral living in the East Atlantic and in the Mediterranean Sea where, under proper circumstances, it can form large populations known as coral forests. Although these coral forests represent vulnerable marine ecosystems of great importance, these habitats are still poorly known, and their monitoring is almost non-existent to date. For this reason, we compared two different models to infer the age of E. verrucosa based on nondestructive measurements of the colonies’ size, in order to highlight strengths and weaknesses of the existing tools for a potential application in long-term monitoring. We also applied the two models on a case-study population recently found in the northwest Mediterranean Sea. Our results showed which model was more reliable from a biological point of view, considering both its structure and the results obtained on the case study. However, this model uses solely the height of the colonies as proxy to infer the age, while the total branch fan surface area could represent a more appropriate biometric parameter to monitor the size and the growth of E. verrucosa. Keywords: Anthozoa; gorgonian; corals; coral habitat; coral forest; VME; mesophotic; modeling; biometry; Mediterranean 1. Introduction The pink sea fan Eunicella verrucosa (Pallas, 1766) is an octocoral species (order Alcyonacea, family Gorgoniidae) living in the East Atlantic, from Ireland to Angola, and in the Mediterranean Sea [1–5]. This species can be found at a depth of 2 to 60 m in the Atlantic Ocean, while it can reach a depth of 200 m in the Mediterranean Sea [1,4–7]. Under proper oceanographic conditions including strong currents and temperate/cold waters, E. verrucosa can form large colony aggregations known as coral forests, settling on hard bottoms sometimes covered by a thin sediment veneer [5]. Similar to other animal forests (sensu [8]), octocoral assemblages provide biomass, structural complexity and aesthetic value to coastal communities, sustaining a rich biodiversity [5,9–17]. Coral forests, comprised of E. verrucosa represent a Vulnerable Marine Ecosystem (VME) because of their vulnerability to human pressures, according to the Food and Agricultural Organization (FAO) [18,19]. This vulnerability is based on the rarity, the functional significance, the fragility (both physical and functional), and the structural complexity of the coral forest, as well as the species’ life-history traits (e.g., slow growth rate, late age of maturity, low or unpredictable recruitment, and extended life expectancy) that makes recovery difficult after a fishing impact. Indeed, bottom-contact fishing gears such as trawl nets, dredges, longlines, and artisanal fishing nets (e.g., gillnets and trammel nets) can have both direct and J. Mar. Sci. Eng. 2020, 8, 951; doi:10.3390/jmse8110951 www.mdpi.com/journal/jmse J. Mar. Sci. Eng. 2020, 8, 951 2 of 12 indirect impacts on these coral forests, representing one of the main anthropogenic threats together with pollution and climate change [5,20–26]. Furthermore, the stranding of E. verrucosa has been recently documented on the southwest coast of England, where the coral appeared to be entangled in lost fishing gears, as well as in domestic marine litter [23]. From the 1960s to the 1970s, colonies of E. verrucosa were collected as souvenirs in the northeast Atlantic, where the species has been currently protected from intentional damage [27]. It represents a major heritage species [28,29] and it is listed as “vulnerable” on the Red List of Threatened Species by the International Union for Conservation of Nature and Natural Resources (IUCN) [30]. More locally, the status of E. verrucosa in the Mediterranean Sea seems to be slightly better than elsewhere, as it is listed as “near threatened” according to IUCN [31]. In fact, records of E. verrucosa are increasing in this basin thanks to the implementation of deep diving techniques, the carrying of Remotely Operated Vehicle (ROV) explorations, as well as the application of a citizen science approach involving scuba divers and fishermen [5–7,25]. The emerging picture is that of a species widespread in the Mediterranean Sea, although large populations constituting coral forests are still poorly known [5]. Due to its vulnerability and ecological importance, E. verrucosa is receiving increasing attention and, similar to other forest-forming corals, further studies are likely to unveil new populations of this species in the mesophotic zone. Together with the finding of new coral forests aiming to assess the overall distribution of these VMEs, their monitoring is essential to understand ongoing and future changes (both natural and anthropogenic) [32]. Underwater observations and size measurements carried out on living colonies have allowed the development of two almost contemporary and independent models of growth and size/age relationship for E. verrucosa, one in the Atlantic Ocean [33] and one in the Mediterranean Sea [6]. In this study we compared the two existing models to infer the age of E. verrucosa based on the size of the colonies, in order to analyze pros and cons for long-term monitoring. Moreover, we applied the two models on a recently described forest of E. verrucosa in the northeast Mediterranean Sea [5] as a case study. New indications to improve age modeling and to obtain more reliable data on E. verrucosa populations are also provided. 2. Materials and Methods 2.1. Models Considered We considered two different models for the correlation of size and age in E. verrucosa. Model A [33] was developed based on 70 colonies tagged and surveyed between 2006 and 2008 in the Gulf of Morbihan (northwest Atlantic coast of France), at a depth of 8–20 m. The authors measured the colonies with in situ photographic recordings, and then used imaging analysis to estimate the total Branch Fan Surface Area (BFSA, cm2), namely, the measure of the surface that is occupied by the organism on photographs in two-dimensional (2D) projection (Figure1). The BFSA was calculated considering both height and width, and linearly correlated to the BFSA with different coefficients (Figure2a,b). A correction factor for branch overlapping was introduced considering that E. verrucosa colonies could exhibit a three-dimensional (3D) morphology. Individual growth was assessed by measuring the increase in the BFSA of tagged colonies during the three years of study, and the following model that correlated the age of the colony with the BFSA was proposed (Figure2a) [33]: BFSA = 1.25 age1.73. (1) × J. Mar. Sci. Eng. 2020, 8, x FOR PEER REVIEW 3 of 13 J. Mar. Sci. Eng. 2020, 8, 951 3 of 12 J. Mar. Sci. Eng. 2020, 8, x FOR PEER REVIEW 3 of 13 Figure 1. Colony of Eunicella verrucosa with indication of height, width, and branch fan surface area (BFSA). Figure 1.1. Colony of Eunicella verrucosa with indication of height, width, and branch fan surface area (BFSA).(BFSA). (a) (b) Figure 2. Model A [33(].a) (a) Estimated behavior of the BFSA (branch fan( surfaceb) area) versus age Figurein Eunicella 2. Model verrucosa A [33]. ;((a)b Estimated) Linear correlation behavior of between the BFSA the (bra BFSAnch and fan heightsurface (blue) area) orversus width age (red) in of EunicellatheFigure colonies. verrucosa 2. Model; ( bA) [33].Linear (a )correlation Estimated betweenbehavior theof theBFSA BFSA and (bra heightnch (blue)fan surface or width area) (red) versus of theage in colonies.Eunicella verrucosa; (b) Linear correlation between the BFSA and height (blue) or width (red) of the The model was based on colonies having an initial BFSA between approximately 3 and 50 cm2. colonies. TheThe latter model size was corresponded based on colonies to an estimated having an age initial of about BFSA 30 between years and approximately an estimated height3 and 50 of cm 282 cm.. The same study reported the following linear relations between BFSA and height (h) and width The latterThe size model corresponded was based to on an colonies estimated having age of an about initial 30 BFSA years between and an estimated approximately height 3 ofand 28 50cm. cm 2. (w) (Figure2b), that have been considered in this study: TheThe latter same size study corresponded reported the to followingan estimated linear age relations of about between 30 years BFSAand an and estimated height ( hheight) and widthof 28 cm. (w) (FigureThe 2b), same that study have reported been considered the following in this linear study: relations between BFSA and height (h) and width h = 0.02 BFSA + 18.08. (2) (w) (Figure 2b), that have been consideredℎ = 0.02 in ×this× study: + 18.08, (2) wℎ= =0.03 0.02 ×BFSA + 14.29. + 18.08, (3) × (2) = 0.03 × + 14.29. (3) Model B [6] was developed based on 15 colonies surveyed every two years between 1997 and 2006 = 0.03 × + 14.29. inModel the Riou B [6] archipelago was developed (Mediterranean based on coast15 colonies of France), surveyed at a depth every between two years 20 and between 40 m. 1997 The authorsand (3) measured in situ the maximum height of the colonies (between 5 and 40 cm) using a decimetre with 2006 in theModel Riou B archipelago[6] was developed (Mediterranean based on coast15 colonies of France), surveyed at a depth every between two years 20 between and 40 m.
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